BRAIN RESEARCH

ELSEVIER Brain Research 740 (1996) 193 200

R e s e a r c h r e p o r t

The effect of satiety on responses of gustatory neurons in the amygdala of alert cynomolgus macaques

J i a n q u n Y a m T h o m a s R. S c o t t *

Department of Psychology and Program in Neuroscience, Unil'ersily of Delaware, Newark, DE 19716 USA

Accepted 9 July 1996

Abstract

An alert cynomolgus macaque was fed a sweet solution to satiety as the activity of a gustatory neuron in the amygdala was recorded to that solution and to four other taste stimuli. This exper iment was conducted a total o f 14 t imes in two monkeys. The responses of

individual neurons to the satiety stimuli were suppressed by as little as lC~, and as much as 100% by the induction of satiety (mean suppression = 58%). Nine of the 14 cells responded to the satiety solution with excitation, and their responses were suppressed by a mean of 62% by satiety. Five neurons responded with inhibition, and their responses were suppressed by a mean of 50~}. Responses to other taste stimuli, not associated with satiety, were affected to a lesser extent. The amygdala is a taste relay between the primary gustatory cortex, where satiety has no influence on responses to taste stimuli, and the lateral hypothalamic area where the effect of satiety is total. The data presented here indicate that the amygdala is a functional as well as anatomical intermediary between these two areas, and serves as a stage in the process through which sensory stimuli are imbued with motivational significance.

Kevwords: Macaque: Monkey: Taste: Amygdala; Satiety: Flavor

1. Introduct ion

The motivation that sustains feeding is provided largely by the palatability of food, including its taste. Therefore, it is appropriate that taste-responsive neurons are scattered throughout regions whose activity is associated with the control of feeding, including the lateral hypothalamic area (LHA) and substantia innominata (SI). Here, taste-sensi- tive neurons respond to a stimulus only when a monkey is hungry and motivated to consume it [4]. This modulation of sensitivity m the very system that helps guide feeding is an economical mechanism for controlling intake. Indeed, one approach lo the study of feeding is to discover which taste cells are susceptible to the influence of satiety, and so may be inw)lved in determining the animal's motivation to consume a potential food.

A diagram of central taste projections in the macaque monkey is shown in Fig. I. The first central relay is in the rostral division of the nucleus tractus solitarius (NTS), in close proximity to visceral afferents that terminate in the

~ Corresponding author. 201 Elliott Hall, University of Delaware. Newark, DE 19716, USA. Fax: + 1 (302) 831-6398; e-mail: thomas.scott@ mv~.udel.edn

adjacent caudal part of the nucleus. One hypothesis is that visceral information could impinge on taste sensitivity even at this early stage of taste processing, as has been demonstrated in the rat [7-10]. This is apparently not the case, however, for taste responses were unmodified in NTS as monkeys were fed to satiety [40]. NTS gustatory neurons project to the parvicellular division of the ventro- posterior medial nucleus of the thalanms (VPMpc) where the influence of satiety has not been investigated. These third-order cells send axons to primary taste cortex situated in the frontal operculum (FO) and continuing to the adja- cent anterior insula (AI). As in NTS, taste-responsive neurons in FO [31] and AI [39] were not influenced by the monkey's level of satiety. Cells in A I / F O project both to secondary taste cortex in the caudolateral orbitofrontal cortex (OFC) and to the lateral, basal, and central nuclei of the amygdala [38]. Both these areas then send fibers to the lateral hypothalamic area, from which they are recipro- cated [1,2]. In OFC, as in LHA, neurons responded to a palatable taste only when the monkey was motivated to consume it [32]. With increasing levels of satiety, the taste-induced response declined, to disappear when the monkey was replete. The susceptibility of amygdaloid taste cells to level of satiety is not known.

0006-8993/9~/$15.00 Copyright ~_'~ 1996 Elsevier Science B.V. All rights reserved. PII S0006- 8 ~)9 ~,(96 )0()864 • 5

194 J. Yah, T.R. Scot t /Brain Research 740 (1990) 193 200

The amygdala is associated with control of emotion, motivation and hedonic tone (reward) [1,16,27]. It is char- acterized as a region where representations of the internal and external worlds overlap, permitting the animal to assess its needs in relation to the external resources avail- able to fulfill them [38]. In this role, the amygdala is involved in the initiation and guidance of feeding, which relies on the integration of visceral and exteroceptive information [17-19,23]. Accordingly, normal feeding is disrupted by amygdaloid lesions in monkeys [11,13] and in humans [12,24]. Specifically, hypophagia and weight loss have been reported to accompany lesions of the central and medial nuclei of rats [3,5,14] and dogs [18], whereas the opposite results from basolateral damage [5,6].

Feeding behavior is largely guided by the sense of taste. Involvement of the amygdala in the control of feeding implies its sensitivity to gustatory input, an implication now conf i rmed by e l ec t rophys io log ica l studies

[25,26,33,34]. Taste-responsive neurons compose approxi- mately 7% of the cells in the central nucleus of the amygdala [34]. Some 80% of these have low levels of spontaneous activity and are excited by taste stimuli: the remainder respond primarily with inhibition fi'om high spontaneous rates. The purpose of this study was to deter- mine the degree to which taste-evoked activity in the central nucleus of the amygdala of macaques was affected by the animal's level of satiety.

2. Methods

2.1. Recording

Two male cynomolgus monkeys, Macaca fascicularis, weighing 4.0-6.0 kg were implanted under sodium pento- barbital anesthesia (2 ml, i.m., preceded by tranquilization

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Fig. 1. Schematic representation of transverse sections summarizing the afferent limb of central gustatory projections in the cynomolgus macaque. Abbreviations: AC, anterior commissure; Ace, nucleus accumbens; Am, amygdala: Ca, caudate: CI, claustrum; CP, cerebellar peduncle: GP, globu.~ pallidus; Hyp, hypothalamus; l, insula; IO, inferior olive; Lf, lateral fissure; LGN, lateral geniculate nucleus; NC, cuneate nucleus; NTS, nucleus of the solitary tract: O, operculum; OC, optic chiasm; OFC, orbitofrontal cortex; OT, optic tract: Put, putamen; SN, substantia nigra; T, thalamus: TL temporal lobe; V, ventricle: VPMpc, ventroposterior medial nucleus, pars parvicellutaris.

J. Yan, T.R. Scott/Brain Research 74(9 (1996) 19,7-200 1c)5

with ketamine at 10 m g / k g , i.m.) with stainless-steel holders on which a Kopf adaptor was fitted during record- ing sessions. After 10 days recovery, daily recording ses- sions were initiated. Single neuron activity was recorded using glass-coated tungsten microetectrodes [20], while the monkey sat in a primate chair with his head restrained to provide recording stability. The electrode was protected by a stainless-steel guide tube which ended just below the anesthetized dura (0.1 ml Lidocaine). The signal from the microelectrode was filtered and amplified by conventional techniques, displayed on an oscil loscope and stored on magnetic tape for subsequent analysis. Monkeys had ad libitum access to water and monkey chow.

A neuron was classified as taste-responsive if it gave an evoked discharge rate > 1.65 S.D.. (0.10, two-tailed) re- moved from its spontaneous rate on each of three succes- sive applications of at least one of the five stimuli. There- fore, the risk of a false positive was 5 × 0.13 = 0.005.

Single-neuron activity was analyzed on an IBM com- puter. Mean discharge rates were calculated for 3 s prior to, and 3 s after each stimulus presentation.

2.2. Stimuli aml stimulus delit'erv

Four basic taste stimuli plus water and the satiating stimulus were applied to the tongue during the recording session. The prototypes of the four basic tastes were presented at moderate-high concentrations as determined from intensity-response functions in the primary taste cor- tex of macaques [35,36]. These were 0.5 M sucrose, 0.3 M NaCI, 0.01 M HC1, and 0.001 M quinine HC1. The satiat- ing stimulus was 20% cranraspberry juice (Ocean Spray) on seven occasions, 1.0 M glucose on four, 0.5 M sucrose twice, and 0.01 M aspartame once. Cranraspberry juice was also used in each experiment as a searching stimulus because of its high palatability and the complexi ty of its taste, such that it was readily accepted by the monkeys and also activated a diverse set of gustatory neurons. Stimuli were delivered through a hand-held syringe in quantities of approximately 0.75 ml. Manual delivery was used to main- tain replicable gustatory stimulation of a large and nearly constant receptive field throughout a recording session despite different mouth and tongue positions adopted by the monkeys as the palatability of the solutions varied with the stimulus quality and level of satiety.

2.3. Requirements /or conducting a satie O' experiment

Fourteen satiety experiments were performed at differ- ent sites within the central nucleus of the amygdala. Each was separated from the others by at least 2 days so as to permit the effects of repletion to dissipate. In order to initiate a satiety experiment three conditions had to be satisfied. I. Gustatory responsil,eness to the satiating chemical. The

neuronal response elicited by application of the stimu- his which would subsequently be used to satiate the

2.

.

monkey had to be robust, whether excitatory or in- hibitory. Satiety was induced by cranraspberry juice, glucose, sucrose, or aspartame. Therefore, the neurons studied in these experiments responded well to stimuli that humans describe as predominantly sweet. Recording stability. After a neuron had been isolated in the amygdala, the stability of the recording and of the evoked response were tested periodically over the next 3 0 - 6 0 rain before a decision was made to begin the experiment. At'idity./or the satiating chemical. A series of objective criteria for the avidity of acceptance has been devel- oped [30]. A satiety experiment was not initiated unless a monkey ' s behavior warranted a rating of at least + 1.0 on a scale of + 2.0 (acceptance) to - 2 . 0 (rejec- tion) (see below). In practice this required an efficient search for a taste neuron in the amygdala and the achievement of a stable recording with a minimum of stimulus presentations, so that the monkey was still avid when the experiment began.

2.4. Criteria.for acceptance or rejection

Scores on the scale of acceptance or reiection were based on the following behavioral criteria:

+ 2.0: maximal acceptance - reaching for the solution with hands and mouth; avid licking. + 1.0: clear acceptance opening the mouth; licking and swallowing the solution. 0.0: neutrality - swallowing the solution when placed in the mouth; absence of avidity: no attempt made to obtain the solution. - 1 . 0 : clear rejection - pursing the lips to prevent administration of the solution: failure to swallow all the solution placed in the mouth. - 2 . 0 : maximum rejection - pursing the lips and closing the teeth; using the tongue to eject delivered solution: swallowing little: using the hands to push the sohltion away. If the behavior was intermediate between these types,

then intermediate scores were given.

2.5. Protocol

If the criteria for conducting a satiety experiment were satisfied, the following protocol was invoked. I. The gustatory neural response to each of the six stimuli

four prototypes, the satiating stimulus, and water - was determined by application of 0.75 ml of each solution. Each application was followed by a 1.0 ml water rinse and a minimum period of 30 s of rest. The stimulus series was then repeated. The total testing time was approximately 12 rain, and the volume consumed was a maximum of 16 ml.

2. The monkey ' s acceptance-rejection score for the satiat- ing solution was determined by observing his response as 0.75 ml was applied to the tongue.

1 9 6 J. Yan, T.R. S c o t t ~ B r a i n R e s e a r c h 740 (1996) 1 9 3 - 2 0 0

3. The monkey was fed a 50-ml aliquot of the satiating solution, delivered orally through a syringe. The dura- tion of administration was approximately 2 min for the initial aliquot and as much as 4 min for the last.

4. The monkey's acceptance-rejection score to the satiat- ing solution was reassessed.

5. Steps (1-4) were repeated through as many cycles as were required to obtain a behavioral score of - 1.5 to - 2 . 0 . This typically involved five (range = 3 to 7) 50-ml aliquots over a period of 60 min. Conventional satiety, defined by the stage at which the subject would stop working to obtain food, would normally corre- spond to a rating of 0.0 to - 0.5. Thus the feeding used in these experiments was sufficient to produce a com- plete level of satiation. After satiety was reached, and eating had stopped, multiple further measurements were taken of the neuronal responses to each of the sapid solutions and to water.

2.6. Localization o f recording sites

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f igure; those that re sponded wi th inhibit ion are in the b o t t o m half.

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sites could then be reconstructed to within 250 /xm by reference to bony landmarks. Secondly, in the final several tracks, microlesions were made through the recording elec- trodes (60 ,aA for 60 s, electrode negative). After the final experiment, monkeys were tranquilized with ketamine (10 mg/kg, i.m.) and deeply anesthetized with sodium pento- barbital (30 mg/kg, i.v.). They were perfused with 0.9% saline followed by formal-saline. The brains were placed in sucrose formalin for at least 7 days, after which 50 ,am serial frozen sections were cut and stained with neutral red.

3. Results

3.1. Overview

The effect of satiating the monkeys was tested on 14 neurons. Nine cells gave excitatory responses to the satiat- ing stimulus and five responded with inhibition. The effect

,1. Yan, T.R. Scott/Brain Research 740 (1996) 193 200 197

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Fig. 4. Responses of three neurons that were initially inhibited by the satiety stimulus, as a function of volume presented. A: suppression of 93%: B: suppression of 70%; C: suppression of 1%.

of satiety was idiosyncratic to each neuron. The responses of some were completely suppressed, those of others par- tially reduced, and the activity of still others was unaf- fected. Across all cells, the mean response declined by 58% (62% for the excitatory neurons and 50% for those that responded with inhibition). The effect was specific to the satiating stimulus: responses evoked by other tastants were not significantly affected by the induction of satiety.

3.2. Spontaneous actir i tv

During the course o f inducing satiety, spontaneous ac- tivity changed only marginal ly . The mean rate increased from 4.9 to 5.4 s p i k e s / s in excitatory neurons, and de- c l ined from 13.9 to 1 1.6 s p i k e s / s in those that responded to the satiating solut ion with inhibit ion. Neither change was statistically significant.

3.3. Eroked responses to the satiating stimulus

The anaount of suppression from before the first aliquot to after the final one was as little as I%, as much as 100%. The initial responses of nine of the fourteen neurons were suppressed by more than 50% during the course of satiety - six of the nine excitatory cells, and three of the five that responded with inhibition. The percent by which the final

response of each neuron was suppressed to the satiety stimulus is plotted in Fig. 2. The responses of six neurons, and the level of acceptance shown by the monkey at each stage of the satiety process are shown in Figs. 3 and 4. Fig. 3 highlights responses of three of the nine excitatory cells, depicting total (Fig. 3A), partial (Fig. 3B), and minimal (Fig. 3C) suppression. Fig. 4 shows responses of three of the five inhibitory neurons, with near total (Fig. 4A), partial (Fig. 4B), and minimal (Fig. 4C) suppression of the inhibition. The mean response among all excitatory and all inhibitory neurons as a function of level of satiety is shown in Fig. 5. Both excitatory and inhibitory responses tended toward spontaneous levels of activity as satiety was induced. The mean excitatory response was reduced by 62%, inhibition by 50%. The mean overall reduction across all fourteen neurons was 58%.

There was no tendency for the degree of suppression to be associated with particular satiety st imuli . Responses to

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198 J. }/an, T.R. Scot t /Brain Research 740 (1996) 193-200

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Fig. 6. Degree of response suppression to the satiety stimulus as a

function of the location of each neuron. Circles mark the location of cells that responded with excitation, and squares, those that gave inhibitory responses. The degree of suppression is represented by the proportion of the symbol that is filled. Abbreviations: Acc, nucleus accumbens; Amyg, amygdala; B, diagonal band of Broca; CA, anterior commissure; Cd, caudate nucleus; ChO, optic chiasm; C1, claustrum; GP, globus pallidus; Put, putamen.

cranraspberry juice were suppressed by a mean of 61 :k 42% (n = 7 ) , those to glucose by 48_+ 29% (n = 4 ) , to sucrose by 72% (n = 2) and the lone response to aspar- tame by 59%.

3.4. Topographic organization

There was no apparent relationship between the position of the neuron and its tendency toward excitation or inhibi- tion nor on the effect of its response to the satiating stimulus. In Fig. 6, the locations of the 14 neurons are plotted as a function of whether their responses were excitatory (circles) or inhibitory (squares), while the de- gree to which their responses were suppressed by satiety is indicated by the proportion of the symbol that is filled.

3.5. Responses to other taste stimuli

While the effects of satiety were greatest for the satiat- ing stimulus, there was some generalization to other taste qalities. Responses to sucrose declined from a mean of 3.7 s p i k e s / s to 3.0 s p i k e s / s (19%; cf. Fig. 7) across all 12 cells for which it did not serve as the satiety stimulus. However, in the neurons whose responses were suppressed by > 50cA to the satiaty stimulus (n = 8), the response to sucrose declined from 3.2 s p i k e s / s to - 0 . 2 s p i k e s / s with satiety; in the four neurons whose responses were sup- pressed < 50%, the mean response to sucrose did not change. Similarly for responses to HC1 and quinine, the responses to which declined in the nine cells most affected by satiety, but not in the five least affected. Low reponse rate and high variability, however, rendered these differ- ences non-significant.

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J. Yan, T.R. Scott/Brain Research 74011996) 193 200 199

4. Discussion

4. I. The role ,.;,f the amygdala in satieO'

Taste cells in insular-opercular (primary) cortex are not influenced by the monkey's satiety or motivation to eat [31,39]. The activity elicited by a sugar solution is identi- cal regardless of whether the monkey is hungry and moti- vated to consume it, or fully satiated and rejecting it. In the lateral hypothalamic area, the opposite is true. Cells re- spond well to the taste of a food if the monkey is hungry, but activity declines to spontaneous levels as he consumes the food to satiety [4]. Thus, neurons that project taste activity to the amygdala presumably code for taste quality regardless of the monkey's motivational state; those that receive taste projections from the amygdala code for level of motivation associated with a particular taste quality. We report here that the taste relay between these two areas contains neurons whose responses are suppressed to vary- ing degrees, with a mean of 58%, making the amygdala a functional as well as anatomical intermediary.

An analogous situation obtains in the visual system. The responses of neurons in inferotemporal cortex to a visual stimulus for food are divorced from a monkey's motivation to obtain that stimulus [30]. These cells project to the amygdala, the activity of whose neurons is partially influenced by motivation to obtain the food [33], then to the lateral hypothalamic area where responses are totally dependent on the motivating value of the food reinforcer [29]. Therefore, the amygdala may serve as one stage in the pathways that imbue sensory information with rein- forcement and motivational significance.

4.2. Taste iersus /laz:or

Gustatory neurons in insular-opercular cortex receive only minor inputs from other senses [28]. Accordingly, taste-evoked activity here provides the closest match of all relays tested to descriptions of taste quality offered by humans in psychophysical studies [15]. The implication is that primary taste cortex is the site of quality identification, scarcely modified by afferents of other senses or by the physiological condition of the monkey.

Similarly, relays that represent advanced stages of pro- cessing in vision (inferotemporal cortex) and olfaction (pirifornl cortex) contain neurons devoted to their respec- tive senses.

Extensive interactions among taste, olfaction and vision occur in the same areas where neurons are affected by satiety: The orbitofrontal cortex, amygdala, and lateral hypothalamic area. To the limited degree tested, the multi- ple modalities that impinge on a cell in these areas are in register, i.e.. if a neuron responds only to a taste that humans describe as sweet, it will be activated only by odors that are sweet, and by the sight of only the syringe that contains a sweet stimulus. This dichotomy between

discrete sensory processing unmodified by physiological state, versus overlapping sensory representations of the same stimulus, may provide the distinction between taste (or olfaction or vision) and flavor. In psychophysical tests, the former is only marginally affected by feeding a human subject to satiety, while the latter is drastically modified [21,22,37]. Tastes are typically reported in descriptive terms while flavors carry hedonic tags (e.g. a sweet taste versus an appealing flavor). The sweetness of the taste, presumably represented in isolation from other senses in primary taste cortex, remains as satiety is induced, while the appeal of the flavor, perhaps coded by multimodal inputs to orbitofrontal cortex, amygdala and lateral hypo- thalamus, declines in parallel with the responsiveness of their neurons.

Acknowledgements

We thank Dr. Barbara K. Giza for assistance in prepar- ing the figures. This research was supported by grant number IBN-9120611 from the National Science Founda- tion.

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