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Rats Relearn a Sodium Chloride vs. Potassium Chloride Discrimination after Chorda Tympani Transection Using Remaining Gu...

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Permanent Link: http://ufdc.ufl.edu/UFE0020978/00001

Material Information

Title: Rats Relearn a Sodium Chloride vs. Potassium Chloride Discrimination after Chorda Tympani Transection Using Remaining Gustatory Input
Physical Description: Mixed Material
Copyright Date: 2008

Record Information

Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: All rights reserved by the source institution and holding location.
System ID: UFE0020978:00001

Permanent Link: http://ufdc.ufl.edu/UFE0020978/00001

Material Information

Title: Rats Relearn a Sodium Chloride vs. Potassium Chloride Discrimination after Chorda Tympani Transection Using Remaining Gustatory Input
Physical Description: Mixed Material
Copyright Date: 2008

Record Information

Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: All rights reserved by the source institution and holding location.
System ID: UFE0020978:00001


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RATS RELEARN A SODIUM CHLORIDE VS. POTASSIUM CHLORIDE
DISCRIMINATION AFTER CHORDA TYMPANI TRANSACTION
USING REMAINING GUSTATORY INPUT


















By

GINGER BLONDE


A THESIS PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF SCIENCE

UNIVERSITY OF FLORIDA

2007

































2007 Ginger Blonde









TABLE OF CONTENTS

Page

L IS T O F T A B L E S ........................................................................... 4

LIST OF FIGURES .................................. .. ..... ..... ................. .5

A B S T R A C T ......... ....................... .................. .......................... ................ .. 6

CHAPTER

1 INTRODUCTION ................................................... ..............................8

2 M E T H O D S ............................................................. ...... .......................................... 1 1

S u b je cts ...................................................................................................... . ...... 1 1
A p p a ra tu s ................................................................ ................................................1 1
T ria l S tru ctu re ................................................................................................................... 12
T raining ....... ............................................................... 12
P re su rg ic al T e stin g ........................................................................................................... 13
Postsurgical Testing................................................. 14
S u rg e ry ................... ...................1...................4..........
H isto lo g y ................... ...................1...................5..........
D ata A analysis ................................................... 16

3 R E S U L T S ..............................................................................................18

H isto lo g y ................... ...................1...................8..........
B behavioral Testing ................................................. 18
W after C o n tro l T e st ........................................................................................................... 19

4 D IS C U S S IO N ........................................................................................................2 5

L IST O F R E F E R E N C E S ..................................................................................................... 3 1

B IO G R A PH IC A L SK E T C H ................................................................................................... 36









TABLE
Table page


2-1 Training and Testing Param eters ............................................... ............................ 17









LIST OF FIGURES

Figure page

3-1 Overall performance during presurgical testing ..................................... .................21

3-2 Overall performance during initial postsurgical testing..................................................22

3-3 Overall performance during postsurgical control and amiloride sessions.........................23

3-4 W after control test .................. .................. ................. ............ .. ............. 24









Abstract of Thesis Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Master of Science

RATS RELEARN A SODIUM CHLORIDE VS. POTASSIUM CHLORIDE
DISCRIMINATION AFTER CHORDA TYMPANI TRANSACTION
USING REMAINING GUSTATORY INPUT

By

Ginger Blonde

May, 2007

Chair: Alan Spector
Major: Psychology

When the chorda tympani nerve (CT), which innervates taste buds in the anterior tongue,

is transected, the ability of rats to discriminate sodium from nonsodium salts is severely affected

but remains above chance. In a recent study, rats lacking input from the CT were initially

impaired but able to significantly improve in an NaCl vs. KC1 discrimination with continued

testing. This study was designed to determine what remaining gustatory input supported the

improvement. Rats were presurgically trained and tested in a two-response operant task to

discriminate NaCl and KC1 on the basis of taste. They were then split into five groups: CT

transaction, (CTx, n=7); CT and glossopharyngeal nerve (GL) transaction, (CTx+GLx, n=4); CT

and greater superficial petrosal nerve (GSP) transaction, (CTx + GSPx, n=8), or sham surgery

(SHAM, n=7; and SHAM-INT, n=7). SHAM-INT rats were tested postsurgically with lower

stimulus concentrations to determine whether the decrease in performance was due to a reduction

in stimulus intensity after surgery. In the first week of postsurgical testing, performance by the

rats with nerve transactions was impaired. However, over the course of six weeks, the CTx and

CTx+GLx groups were able to increase their overall percentage correct to near-presurgical levels

and were affected by amiloride similarly to SHAM rats. The CTx + GSPx group never









improved. Also, the SHAM-INT group performed similarly to the SHAM group throughout

postsurgical testing. Thus, it does not appear that the effect of nerve transactions on performance

can be explained by lower stimulus intensities after surgery. It instead seems that the taste

quality of one or both of the salts changes after CT transaction. However, the signal arising from

the GSP, but not the GL, is sufficiently different between the two salts to allow the rats to learn a

new discrimination.









CHAPTER 1
INTRODUCTION

The chorda tympani nerve (CT), a gustatory branch of the seventh cranial nerve that

innervates taste buds in the anterior tongue, has been shown to be important for normal taste-

guided behavior related to salts. When the CT is transected, detection of salts, particularly NaC1,

discrimination of sodium versus nonsodium salts, expression of sodium appetite, and ingestive

oromotor responses are impaired (e.g., 1-14). In some cases, NaCl preference is also impaired

after CT transaction in the rat (e.g., 15-16), but it has generally been unaffected by the

denervation when measured by intake tests (e.g., 14, 17).

Electrophysiological findings show that in rodents the CT is highly responsive to salts,

especially sodium salts (e.g., 18-25). A subpopulation of nerve fibers in the rodent CT, called N-

fibers, responds robustly and specifically to sodium salts relative to other tastants. In contrast, a

separate subpopulation called H-fibers is more electrolyte-general, responding to both sodium

and nonsodium salts as well as acids and quinine (26-30). Additionally, taste buds in the

fungiform papillae contain epithelial sodium channels (ENaCs) that are thought to be the primary

transduction mechanism for sodium detection. Lingual application of amiloride, which blocks

ENaCs, diminishes responsiveness of the CT in general, and N-fibers in particular, to sodium

salts. There seems to be little effect on the CT response to KC1, or responsiveness of H-fibers,

with the addition of amiloride. The distinct N-fiber transmission pathway specifically

representing sodium in the periphery, as compared to the more general H-fiber pathway for

electrolytes, seems to be the basis for NaCl vs. KC1 discriminability, and the CT incorporates

both pathways (e.g., 28-29, 31-33). The results of behavioral and electrophysiological studies all

suggest that the CT is important for salt detection and discrimination in rats.









Most of the behavioral studies described above tested animals over a short period of time

postsurgically. In one previous study in our laboratory, rats with a bilaterally transected CT

performed poorly postsurgically in a NaCl versus KC1 discrimination, as seen in other

experiments. However, with longer testing, some rats were able to improve their overall

performance in the task, approaching presurgical levels (34). This suggests that the remaining

gustatory input is capable of providing sufficient information to the rat, allowing it to accurately

perform the discrimination when provided adequate postsurgical testing to relearn the task.

Indeed, even after CT transaction, some degree of sodium detectability remains. It has

been suggested that the greater superficial petrosal nerve (GSP), the branch of the seventh cranial

nerve that innervates taste buds in the nasoincisor ducts, geshmacksstreifen, and soft palate in the

rat, is responsible for the remaining ability of rats to perform these tasks after CT transaction.

Electrophysiological recording experiments have shown that the GSP also responds well to salts,

although it responds best to sugars (22, 35-36). Additionally, the taste bud fields innervated by

the GSP seem to contain ENaCs; lingual application of amiloride decreases overall GSP

responsiveness to sodium salts (36-37).

The results of behavioral studies also suggest that the GSP has a role in taste-guided

behaviors related to sodium. After combined CT and GSP transaction, eliminating all gustatory

input from the seventh cranial nerve, the detection threshold for NaCl and performance on salt

discrimination tasks are more affected than when the CT is transected alone (38-39).

In contrast to the CT and GSP, the glossopharyngeal nerve (GL), a branch of the ninth

cranial nerve which innervates the taste buds of the posterior tongue, has been shown to be

unnecessary in behavioral detection or recognition of sodium by the rat. After the GL is

transected, there is no effect on the specificity or vigor of a depletion-induced sodium appetite,









salt discrimination performance, or intensity difference thresholds for NaCl (13, 40-42).

Electrophysiological findings demonstrate that the GL responds best to bitter-tasting stimuli such

as quinine hydrochloride. It has a weaker response to sodium salts (25, 43-45), and it has been

suggested that the circumvallate taste buds of the rat have no functional ENaCs on the basis that

application of amiloride has no effect on GL responsiveness (46-47; but see 48).

This study was designed to explicitly test whether the GSP, considering its proposed

contribution to salt taste, allowed the rats with CT transaction in our previous study to improve

performance in a NaCl versus KC1 discrimination postsurgically. We also tested whether the

GL, which was also left intact in those rats with CT transaction, was providing sufficient

information to support recovery of performance over the postsurgical testing period. A control

group was included in the design that allowed us to assess whether the decrease in

discriminability is related to a decrease in intensity of the stimuli that would follow after some of

nerve transaction surgeries. We hypothesized that given the electrophysiological response

properties of the GSP along with the fact that combined CT and GSP transaction often has

greater effect on performance than transaction of the CT alone, it is likely that the GSP, and not

the GL, is responsible for the level of performance seen after CT transaction.









CHAPTER 2
METHODS

Subjects

Thirty-six Sprague-Dawley rats served as subjects. The rats were housed individually in

polycarbonate cages during training and testing. While recovering from surgery, rats were

housed in stainless-steel hanging wire cages. The room was maintained with a 12-hr light-dark

cycle with temperature automatically controlled; lights came on at 6:30 a.m. Rats had ad-lib

access to laboratory rodent chow (Rodent Diet 5001; PMI, Brentwood, Missouri) in their home

cages. For one week prior to the start of training, they were given oil mash (5 parts powdered

rodent chow to 2 parts vegetable oil) in preparation for the presentation of this palatable and

lubricated diet during postsurgical recovery. During training and testing, water bottles with

purified water (Millipore Elix 10; Bellerica, Massachusetts) were available Friday afternoon after

the last testing session, until Sunday afternoon when they were removed. Monday through

Friday during training and testing, the rats obtained purified water as part of their 40-minute

testing sessions. Throughout testing, no rat ever dropped below 85% of its free-feeding body

weight. All procedures were approved by the Institutional Animal Care and Use Committee at

the University of Florida.

Apparatus

Training and testing took place in a gustometer described in Blonde et al, 2006 (38).

Briefly, rats were placed in a sound attenuation chamber fitted with a central sample spout

positioned behind an access slot and two reinforcement spouts, one to either side of the sample

spout. A cue light was placed above each reinforcement spout. Stimuli were contained in

pressurized reservoirs connected to solenoid valves calibrated to deliver -5 tL of fluid, and were









delivered through the sample spout after it was initially filled at the start of a trial. After each

trial, the sample spout was rotated over a funnel, rinsed with purified water and blown dry.

Trial Structure

Each trial began when the rat licked the sample spout twice in 250-ms, to ensure that the

rat was engaged in spout licking when the stimulus was delivered. During the sample phase, the

rat was allowed 5 licks of the stimulus or 3-s, whichever came first. The decision phase began

immediately: the sample spout rotated away from the access slot, the house lights were

extinguished and the cue lights illuminated. The rat had 5-s (limited hold) to lick from one of the

two reinforcement spouts. If the rat responded correctly, it received up to 10 licks of purified

water in 8-s from the reinforcement spout. During amiloride sessions, 100 iM amiloride

replaced water in the reinforcement spouts. If the rat responded incorrectly or failed to respond

during the limited hold, it received a 30-s time-out, when all lights were extinguished and it had

no access to water. The reinforcement or time-out was followed by a 6-s intertrial interval,

during which the sample spout was rinsed and dried. The sample spout was then rotated back to

the access slot, the house lights were turned on, and the animal could initiate another trial. The

rats were allowed to initiate as many trials as possible during each 40-min session.

Training

The rats were trained to associate one reinforcement spout with 0.2 M NaCl and the other

with 0.2 M KC1 (both reagent grade chemicals; Fisher Scientific, Orlando, FL). The assignment

was counterbalanced, so that for half of the rats the left spout represented NaC1, and for the other

half it represented KC1. The training and testing schedule is depicted in Table 2-1.









Spout training. The rats were trained to lick each spout. One 40-min session was

devoted to each spout (sample, left reinforcement, right reinforcement), and rats received

purified water ad libitum.

Side training. The rats were trained to associate one reinforcement spout with NaCl and

the other with KC1. In each session, only one stimulus was presented via the sample spout, and

only the reinforcement spout associated with that stimulus was available. The stimulus presented

and the reinforcement spout available was alternated each day.

Alternation. For this phase, both 0.2 M NaCl and 0.2M KC1 were presented in each

session. The rat was required to make a predetermined number of correct responses to each

stimulus before the other stimulus was presented. This criterion number was reduced

systematically over three sessions, from 6 responses to 2.

Discrimination Training I. In this phase, 0.2 M NaCl and 0.2 M KC1 were presented

randomly. The probability of receiving either stimulus was 0.5. The rat was required to perform

>80% overall on trials with a response to move on to the next phase of training.

Discrimination Training II-III. The number of stimuli was increased to six. The

limited hold was systematically reduced, and the time-out was increased. As in Discrimination

Training I, the rat had to perform >80% overall to move on to the next phase.

Presurgical Testing

During presurgical testing, the rats were tested on Monday, Wednesday, and Friday with

0.1 M, 0.2 M, and 0.4 M NaCl and KC1 in control sessions. For the Tuesday and Thursday

sessions, the salt stimuli were dissolved in 100lM amiloride. Testing was conducted for two

weeks, for a total of six control sessions and four amiloride sessions.









Postsurgical Testing

Testing resumed 28-30 days after surgery. For four weeks, animals were tested Monday

through Friday in the same manner as during presurgical control sessions. During weeks 5 and 6

of postsurgical testing, the rats were tested identically to presurgical testing. Three days after the

last day of testing, a water control test was conducted in which all reservoirs were filled with

water. This test helped to determine whether the performance of the rats relied on chemical cues

of the stimuli as opposed to other extraneous cues.

Surgery

Surgical groups were balanced by overall performance, performance to each salt, body

weight, and gustometer. All rats were anesthetized with an intramuscular injection of ketamine

hydrochloride (125 mg/kg body weight) mixed with xylazine hydrochloride (5 mg/kg body

weight). For rats receiving bilateral CT transaction (CTx), the external auditory canal was

retracted and the tympanic membrane was punctured. The chorda tympani was exposed and

transected where it disappears behind the malleus. The ossicles were removed, and the

remaining tympanic membrane as well as the surrounding rim of the ear canal was cauterized,

which generates the production of cerumin that fills the middle ear to reduce the likelihood of

nerve regeneration. For rats receiving bilateral CT and GL transaction (CTx + GLx), the above

procedure was performed to transect the CT. Then, to transect the GL, we retracted the

sublingual and submaxillary salivary glands and the sternohyoid, omohyoid, and posterior belly

of the digastic muscles. The fascia underlying the hypoglossal nerve was dissected near the

external medial wall of the bulla to expose the GL. It was cut with microscissors and

approximately 10 mm of the nerve was removed. The incision was closed with nylon sutures.









For rats receiving bilateral combined CT and GSP transaction (CTx + GSPx), an incision

was made dorsal to the pinna and the external ear was retracted, exposing the ear canal. A small

slit was made in the canal. The fascia was dissected to expose the auditory meatus, and the

surrounding musculature was blunt dissected and retracted. The opening of the bony meatus was

enlarged with a high-speed pneumatic dental drill. The tympanic membrane, ossicles, and CT

were removed. The tensor tympani muscle and a small piece of temporal bone were then

removed with microforceps, exposing the GSP. It was transected, and the ends were cauterized.

The incision was closed with wound clips.

The remaining rats received sham surgery (SHAM, and SHAM-INT). For these animals,

the GL was exposed as described above but not transected. Additionally, an incision dorsal to

the pinna was made, the external ear was retracted, a slit was made in the ear canal, and the

tympanic membrane was punctured.

During recovery, rats were individually housed in hanging wire cages until their incisions

had healed. Each animal received Penicillin G Procaine suspension (30,000 units sc) and

ketorolac tromethamine (2 mg/kg body mass sc) for 3 days following surgery. All rats also

received a supplemental diet of oil mash (5 parts powdered 5001 chow to 2 parts oil) and diluted

sweetened condensed milk (1:1 Carnation sweetened condensed milk to water with 1 mL

Polyvisol multivitamin supplemental drops, Enfamil, Eversville, IN). This diet of oil mash and

milk was provided until the rats had recovered, demonstrated by a stable body weight of at least

90% of an animal's presurgical weight, which took a minimum of 5 and a maximum of 25 days.

Histology

Two to three days after the water control test, the rats were deeply anesthetized with

sodium pentobarbital (60 mg/kg, ip) and transcardially perfused with saline, followed by 10%









buffered formalin. The tongue, soft palate, and nasoincisor ducts of each rat were removed and

stored in 10% buffered formalin. The anterior portion of the tongue from the intermolar

eminence to the tip was placed in purified water for 20 min, dipped in 0.5% methylene blue until

saturated (-30 sec), then rinsed with purified water. The epithelium was removed from the

underlying tissue, pressed between two slides, and the total number of fungiform papillae and

taste pores were counted under a light microscope. The foliate and circumvallate papillae and

the nasoincisor ducts were embedded in paraffin and cut into 10 .im sections. These sections

were mounted on slides, stained with hematoxylin and eosin, and taste buds were counted under

the microscope. All tissue sections were coded so that the counters were uninformed of the

surgical condition.

Data Analysis

The overall percentage correct for trials with a response was calculated. Individual

performance was calculated for control and amiloride sessions (separately for both presurgical

and postsurgical testing). Performance during the first four weeks of postsurgical testing was

compiled by week (4-5 sessions per week) for each animal. These data were compared by group

using matched t-tests and analyses of variance (ANOVAs) with Tukey's honestly significant

difference procedure test. Since the probability of the presentation of either salt was 0.5, chance

performance is considered an overall percentage correct of 50%. Group performance was

compared to chance levels using one-sample t-tests. The performance of each rat on the water

control test was statistically tested for positive differences from chance with the one-tailed

normal approximation of the binomial distribution.










Table 2-1. Training and testing parameters


Phase
Training
Spout
Side
Alternation
Discrimination I
Discrimination II
Discrimination III


LH
Sessions (s)


N/A
180
15
10
10
5


Stimuli


N/A H20
0 0.2M NaCl or KCl
10 0.2M NaC1 and KCl
10 0.2M NaC1 and KC1
20 0.1, 0.2, and 0.4 M NaCl and KCl
30 0.1, 0.2, and 0.4 M NaCl and KCl


Stimulus
Presentation

Constant
Constant
Criteriona
Semi-randomb
Semi-random
Semi-random


Testing
0.1, 0.2, and 0.4 M NaCl and KCl
Presurgical 10 5 30 [with and without 100[tM amiloride] Semi-random
0.1, 0.2, and 0.4 M NaCl and KCl
Postsurgical 29-31 5 30 [with and without 100lM amiloride] Semi-random
Note: LH = limited hold, the amount of time (in seconds) the rat has to respond after sampling
the stimulus. TO = time out (in seconds) for incorrect responses. a: the alternation criteria used:
6, 4, 2. b: Stimuli were presented in randomized blocks of 6 without replacement.









CHAPTER 3
RESULTS

Histology

Stained tissues were semi-quantitatively analyzed to determine the success of surgery. If

it appeared that the taste bud field was not intact (i.e., the nerve innervating it had been

transected), the number of taste buds were counted. Three rats in the CTx + GLx group were

removed because the anterior tongue had more than 30% of its fungiform papillae intact,

indicating some level of CT regeneration in those animals. Their data were not included in the

analyses. One rat in the CTx + GSPx group had 20 taste buds in the nasoincisor ducts; however,

based on its performance it does not appear that the taste buds were sufficient to support

discrimination. The statistical outcomes of the analyses were unaffected by whether this rat was

included or not; therefore, that rat was not discarded. After discarding rats on histological

grounds the final group sizes were CTx, n=7; CTx + GLx, n=4; CTx + GSPx, n=8; SHAM, n=7;

SHAM-INT, n=7.

Behavioral Testing

During presurgical control sessions, all groups were performing at high levels overall

(left panel, Figure 1). Even after the removal of rats due to nerve regeneration, there was no

difference between groups during presurgical control sessions, with no main effect of group in a

two-way ANOVA (F(4,28)=1.87, p=0.144). As expected, the addition of amiloride significantly

decreased performance presurgically (main effect of AMILORIDE: F(1,28)=1927.509, p<0.001;

no effect of the interaction GROUP x AMILORIDE: F(4,28)=0.332, p=0.854; right panel, Figure

1), although performance for the SHAM and CTx groups were significantly higher than chance

(p>0.05 for both).









In the first week of postsurgical testing (i.e., the first 5 sessions), all groups with nerve

transactions were significantly impaired compared to their presurgical performance (all p-

values<0.05; Figure 2). Additionally, rats with CTx and CTx + GLx surgeries were performing

at similar levels to each other (p>0.05). The performance of rats with CTx + GSPx surgeries was

at chance (p = 0.781) and significantly lower than that for CTx and CTx + GLx rats (p<0.021),

suggesting that the GSP was contributing to performance in this discrimination. Rats in the

SHAM-INT group, however, were performing similarly to SHAM animals, despite being tested

with concentrations that were 1.0 logo unit lower (p>0.05). Their performance suggests that the

impairment seen in rats with nerve transactions is not simply due to a reduction in stimulus

intensity after surgery.

By the second week of testing, rats in the CTx and CTx + GLx groups had significantly

improved compared to their performance in the previous week (p<0.035 and p<0.004,

respectively), though those groups still performed below presurgical levels (p<0.05 for both).

They continued to improve slightly throughout postsurgical testing. These two groups were

never significantly different from each other. The CTx + GLx group actually reached

presurgical levels by the start of amiloride testing in Weeks 5 & 6 (p>0.2). Rats in the CTx +

GSPx group, on the other hand, remained at or near chance levels throughout postsurgical testing

(p>0.05 for Postsurgical Weeks 1-4; p = 0.02 during Postsurgical Control sessions; see Figures 2

& 3). As with presurgical testing, all groups performed at or near chance levels when tested with

amiloride (Figure 3). Statistically speaking, the SHAM group was significantly above 50%

overall during amiloride sessions (p<0.001 and p<0.03, respectively), but these groups were

clearly impaired when performance was compared to control sessions (p<0.05 for both).









Water Control Test

Two rats performed significantly better than chance on the water control test (Figure 4).

Performance for those rats, however, was significantly lower than their performance when tested

with chemical stimuli and was very close to chance levels. Also, considering that the CTx +

GSPx rats were all performing at chance levels, it is unlikely that the rats were using a consistent

extraneous cue to guide performance.










PRESURGICAL
CONTROL SESSIONS


I-
w
2 90
O
0
0 80

70
6 70
Z
O 60
50
50


PRESURGICAL
AMILORIDE SESSIONS


GROUP GROUP
Figure 3-1. Performance during presurgical testing.
Overall percentage correct (+ SE) by group for presurgical control sessions (left panel) and
amiloride sessions (right panel). *: group performance was significantly higher than chance
(50% overall) during amiloride sessions.


I II A
-A^' o~o c cA^ o^< ^
st^Ds\ 0^ ^' 0^













POSTSURGICAL
FIRST FOUR WEEKS


-- SHAM
-- SHAM-INT
-- CTx
-- CTx + GLx
-A- 7x


1 2 3 4

POSTSURGICAL
TESTING WEEK

Figure 3-2. Overall performance during initial postsurgical testing.
Mean performance (+ SE) by group on control sessions during postsurgical testing weeks 1-4.










POSTSURGICAL
CONTROL SESSIONS


1J-
(~


-;k G\0


POSTSURGICAL
AMILORIDE SESSIONS


GROUP GROUP
Figure 3-3. Overall performance during postsurgical control and amiloride sessions.
Mean overall performance (+ SE) by group during postsurgical control sessions (left panel) and
amiloride sessions (right panel). *: group performance was significantly above 50% overall
during amiloride sessions.











WATER CONTROL TEST
100
I-

80
^ 80
0
0 60

40
z
o 20
0


RAT
Figure 3-4. Water control test. Overall performance for individual rats during the water control
test. *: performance was significantly greater than 50% overall.









CHAPTER 4
DISCUSSION

The recovery from the impaired performance in salt discrimination, caused by CT

transaction, that occurs with prolonged postsurgical testing clearly depends on the input of the

GSP, not the GL. Not only were CTx + GLx rats able to significantly improve over the six

weeks of postsurgical testing, their overall performance level increased at the same rate as rats in

the CTx group, with an intact GL. This indicates that the GSP is supplying the signal that rats

use to discriminate NaCl from KC1 after input from the CT is lost. Additionally, when rats

lacked input from both the CT and the GSP, they performed more poorly than the CTx and CTx

+ GLx groups, and their performance remained virtually at chance levels during the six weeks of

testing. Thus, the GSP is both necessary and sufficient for the rats to improve in this salt

discrimination task when the CT has been damaged. One caveat, however, is that the superior

laryngeal nerve (SLN, a branch of CN X that in rodents innervates taste buds in the laryngeal

epithelium; see 49-50) remained intact in these rats. Because the CTx + GSPx group performed

at or near 50% throughout postsurgical testing, the SLN is clearly not sufficient for this

discrimination. However, it might play a role, along with the GSP, to support the recovery of

performance shown by the CTx and CTx + GLx groups. Based on the position of the taste buds

it innervates and its general response properties, it has been suggested that the primary role of the

SLN is the protection of the airway (see 51). Although for the reasons stated it is unlikely that

the SLN is contributing to the improvement seen in this study, its contribution cannot be entirely

ruled out at this time.

The chance performance by CTx + GSPx rats in this discrimination corresponds with

other studies done by our laboratory. Rats with this combined CT and GSP transaction also

performed at chance levels when tested with a NH4C1 vs. KC1 discrimination (39). Also, while









still able to detect very high concentrations of NaC1, rats lacking input from both the CT and the

GSP have a higher NaCl detection threshold than rats missing only the CT (38). The results of

this study therefore add to the suggestion in the literature that the seventh cranial nerve is

essential for normal detection and discrimination of gustatory stimuli (see 52).

Additionally, the overall improvement shown by CTx and CTx + GLx rats in this study

seems to require the amiloride-sensitive transduction pathway. With the addition of amiloride,

performance by the CTx and CTx + GLx groups significantly decreased. Moreover, it decreased

to the level seen during presurgical amiloride sessions. This corresponds with the other literature

which suggests that amiloride-sensitive ENaCs are crucial for normal sodium discrimination.

Unlike the GSP, however, the GL seems to be neither necessary nor sufficient. Rats in

the CTx and CTx + GLx groups improved at the same rate, never differing significantly from

each other, suggesting that the GL is not providing a necessary signal. Rats with an intact GL

but without an intact CT and GSP performed at or near chance levels throughout postsurgical

testing, indicating that the GL is also not sufficient. It is possible that the GL would be able to

support performance if tested for a longer period of time; although, given that rats in the CTx +

GSPx group were performing at or near chance for 6 weeks of testing, it is more likely that they

would lose stimulus control before relearning the discrimination. Also, despite the fact that

transaction of the GL has never been shown to affect performance in salt-based gustatory tasks

(13, 40-42), the possibility that the GL could support improvement after CT transaction if other

stimuli were used cannot be dismissed. As an example, transaction of the CT has also been

shown to diminish performance by rats in a KC1 vs. quinine discrimination (52). Because the GL

does not seem to have functional ENaCs in the rat, it is unlikely to support discrimination

involving sodium salts, but it does respond well to bitter stimuli such as quinine hydrochloride.









It is possible that, given the electrophysiological response properties of the GL, it would be able

to provide a discriminable signal to allow overall improvement in that task.

In contrast to groups with nerve transactions, the SHAM-INT group performed similarly

to SHAM animals throughout postsurgical testing, despite receiving considerably lower stimulus

concentrations. Because the SHAM-INT rats were relatively unaffected by decreasing stimulus

concentrations it suggests that the diminished performance by the rats with nerve transactions is

not simply due to a decline in stimulus intensity after gustatory denervation. Rather, it seems

that the rats are effectively learning a new discrimination, possibly because the rats do not

perceive the stimuli the same after the loss of input from the CT. For instance, transaction of the

CT impairs the specific increase in intake of sodium by sodium-deplete rats, indicating that rats

do not recognize sodium as such (7) suggesting, perhaps, that sodium is not perceived the same

by rats after the CT is transected. The same could be true for KC1, but would be more difficult to

determine because there is no comparable depletion-induced specific appetite for potassium.

It should be noted that while there was not a significant effect of decreasing

concentrations on performance in the SHAM-INT group, they were slightly lower than SHAM

rats (Figure 2). It therefore might be true that intensity is having some effect on the impairment

in performance seen in the groups with nerve transactions. However, it would be difficult to test

using lower concentrations for the SHAM-INT rats because there is a risk of dropping further

below the normal threshold for these stimuli. The two lowest concentrations of KC1 for the

SHAM-INT rats are already below the detection threshold for intact rats seen previously in the

literature (1). These rats might actually be using a difference in intensity to discriminate the two

stimuli, since the NaCl concentrations used here are all above the detection threshold of intact

rats (e.g., 2, 38). Also, since detection threshold is technically a statistical term that denotes the









concentration at the midpoint of a psychophysical function, it is also possible that

discriminability continues below that point. The 1 logo unit decrease in stimulus concentrations

for the SHAM-INT rats was designed to emulate the lowered detection thresholds seen after

nerve transaction. As with the SHAM-INT rats, at least the lowest concentration of KCl is below

the reported detection threshold for CTx rats (1). The concentrations of NaCl used are

technically above, but approaching threshold for those rats, as well (e.g., 2). Only 0.4 M NaCl

was above the reported detection threshold for CTx + GSPx rats (38), although KC1 detection has

not been explicitly tested in these rats. As such, all of the groups were tested postsurgically with

some subthreshold concentrations. One might expect, then, that the nerve-transected groups

could show a similar level of performance to the SHAM-INT rats, if the only effect of nerve

transactions were to decrease the stimulus intensity, although it might still not be possible for the

CTx + GSPx group.

Similarly, it would be difficult to increase concentrations postsurgically for the groups

with nerve transactions, since there is a risk of NaCl stimulating the trigeminal system with

higher concentrations (e.g., 53). Thus, intensity cannot be ruled out completely. However, it

remains true that the GSP, and not the GL, is supporting the improvement in performance seen in

CTx rats, and that a decrease in stimulus intensity cannot fully explain the change in

performance postsurgically for rats lacking certain gustatory input.

Indeed, the marked decrease in performance immediately after surgery, followed by a

rapid improvement in both the CTx and CTx + GLx groups is similar to that seen previously in

our laboratory when animals learn a particular discrimination and then are given new stimuli.

Spector and Kopka (2002) initially trained rats to discriminate quinine from KC1, and then

replaced quinine with NaC1. At first, the rats performed poorly to the new NaCl vs. KCl









discrimination, but quickly improved to near the level of their initial testing with quinine (54).

While those rats did not receive nerve transaction surgery, the pattern of performance is similar

to that seen in this study. Given that sodium is an essential nutritional element, it is perhaps not

surprising that even after the loss of input necessary to perform this discrimination normally,

remaining gustatory input would continue to allow the discrimination of sodium salts from

others.

In the future, use of a generalization paradigm, such as presenting test stimuli in a licking

or intake test after presurgically conditioning a taste aversion to either KC1 or NaC1, would help

determine whether the qualitative percepts of these stimuli change after nerve transaction. In

conditioned taste aversions studies, exposure to a novel stimulus is paired with, usually, an

intraperitoneal injection of lithium chloride, which induces visceral malaise. An animal then

associates that stimulus, sometimes after only one pairing, with malaise, and avoids it on

subsequent presentations. Animals will not only ingest less of the conditioned stimulus, but will

also decrease intake of other stimuli; this generalization is thought to be an index of perceptual

similarity between the test stimulus and the conditioned stimulus (e.g., 55-56). It might be

possible to condition an aversion to either NaCl or KC1, and then transect the CT One could

then compare the degree of avoidance in CTx rats to that of SHAM rats, to determine whether

there is some difference after surgery. While this has been done for NaCl in F344 and Wistar

rats, which suggested that there is no qualitative difference in the perception of NaCl after CTx

(57), it has never been tested Sprague-Dawley rats, or for KC1. It should also be noted that the

experiment did not test a wide range of stimuli, which might explain why an effect of CT

transaction was not shown.









These results show that not only is the seventh cranial nerve crucial for normal salt

discrimination, the GSP itself is capable of supporting the relearning of this discrimination after

the CT is damaged. It is unknown whether the GSP is inherently capable of supporting this

discrimination, or if the signal from the GSP is strengthened because it is correlated with the

signal from the CT during presurgical testing, in a form of Hebbian learning (for recent review,

see 58). There is overlap in the terminal fields of the CT and GSP in the nucleus of the solitary

tract, which is the first site of synapse for the gustatory system (e.g., 59). It is possible that in this

area of overlap the strong signal from the CT correlates with a potentially weaker signal from the

GSP during presurgical exposure to the stimuli, strengthening the signal from the GSP. Then,

once the input from the CT is lost, the GSP provides sufficient information for the rats to relearn

the discrimination. One way to test this would be to perform surgery before training, thus

avoiding the presurgical experience. However, given the poor performance by the rats with CT

transactions immediately after surgery, it would probably be difficult to effectively train the

animals at that point.

These results contribute to the body of literature that suggests that the seventh cranial

nerve is necessary for detection and discrimination of taste stimuli, and further indicate that

signals from remaining gustatory nerves can support relearning of a salt discrimination even after

the loss of necessary gustatory input. Further studies should be done to determine whether this

phenomenon extends to other stimuli and nerves, as well as to define the underlying neural basis

for relearning discrimination after nerve damage.









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BIOGRAPHICAL SKETCH

Ginger Blonde was born on July 28, 1982 in Carbondale, Illinois. She grew up in Tampa,

Florida, graduating from C. Leon King High School in 2000. She earned her B.S. from the

University of Florida in Gainesville, Florida, in 2004. She is a member of the Golden Key

Honor Society.

While still an undergraduate, she began working in a Behavioral Neuroscience

laboratory, studying the peripheral gustatory system as it related to taste-guided behavior. She

joined the Psychology Department's graduate program in August, 2004.