Catecholaminergic mechanisms of feeding-related lateral hypothalamic activity in the monkey

The functional role of the catecholaminergic mechanism in the lateral hypothalamus (LHA), in feeding behavior of the monkey was investigated by single neuron activity recording and electrophoretic application of dopamine (DA), noradrenaline (NA) and their antagonists. The feeding paradigm had 4 phases: cue light (CL) signaled start of bar press; bar press (BP, 20-30 times); short cue tone (CT) triggered by last bar press signaled presentation of food; and ingestion-reward (RW). Of 312 neurons tested, 189 (61%) responded in one or more phases of the feeding task. Two types of response were observed: CL- or CT-related transient, and BP- or RW-related long-lasting responses. These feeding-related responses depended on the nature of the food and on the hunger-satiety level. DA excited or inhibited different neurons, while NA mainly inhibited firing. DA-sensitive neurons responded more often in the feeding task than insensitive neurons due mainly to differences in responsiveness to CL on (chi 2 test, P less than 0.01), at motor initiation, and during BP (P less than 0.05). Spiperone blocked the former two responses. NA-sensitive neurons responded more often in the feeding task due to responsiveness during BP and RW (P less than 0.01). Sotalol blocked some BP-related responses, and phenoxybenzamine and sotalol blocked the CT-related responses. The data suggest that dopaminergic and noradrenergic inputs in the LHA are crucial in task initiation and reward processing, respectively. Integration of these catecholaminergic and other inputs in the LHA might be important in accomplishing motivated feeding.     

Neuronal activity in the ventral tegmental area (VTA) during motivated bar press feeding in the monkey

Neuronal activity of 58 dopaminergic (DA) and 200 non-dopaminergic (non-DA) neurons in the ventral tegmental area (VTA) of female monkeys was recorded, and correlation to bar press feeding, sensory stimulation and change in motivation was investigated. DA neurons, judged by duration of action potentials (more than 2.5 ms) and responsiveness to apomorphine, had lower firing rates (0-8 impulses/s); non-DA neurons had intermediate firing rates (10-30 impulses/s). Two-thirds of the DA and non-DA neurons responded in bar press feeding; the former with mostly tonic and the latter with phasic responses. Fifteen neurons (5%) responded phasically to arm extension toward the bar, 124 (excitation 88, inhibition 36, 45%) during bar press (BP), and 91 (excitation 32, inhibition 59, 33%) during ingestion reward (RW). Most BP responses (84/124, 68%) continued tonically throughout the BP period with no correlation to each BP movement. In 14 neurons (14/124, 11%), firing showed a specific variation: transient early BP responses shifted to tonic steady ones in palatable food trials, and the shifts correlated well with BP speed. In 20 other neurons, firing increased during BP hip lifting, and at specific vocalization to ask for food; it decreased during food ingestion, drinking and inguino-crural stimulation. Apomorphine administration decreased firing for the first 5-15 min, then increased it with frequent lip smacking, nausea, involuntary movement and vocalization. Thus VTA neurons showed mostly steady tonic responses but some specific phasic responses. They responded not only to motor events but also in close relation to changes of motivational aspects. Neuronal responses were excitation during procurement of reward and inhibition during or after perception of reward. This modulation in firing, might be important in the initiation and execution of movement and/or motivated behavior.     

Behavioral significance of monkey hypothalamic glucose-sensitive neurons

Feeding-related neuronal activity of lateral hypothalamic glucose-sensitive and glucose-insensitive neurons was investigated in behaving monkeys. The behavioral paradigm was a high fixed ratio of bar pressing for food reward signaled by light and tone cues. Twenty-seven percent of the neurons tested were glucose-sensitive. The population of neurons which changed in firing rate during the feeding task was higher among glucose-sensitive cells than among glucose-insensitive cells. The activity of many glucose-sensitive neurons decreased during the bar pressing and reward periods. A small population of glucose-sensitive neurons responded to cue stimuli. The results suggest that glucose-sensitive neurons are mainly involved in the drive and/or reward mechanism of feeding behavior, and that these cells may have specific roles in neural control of hunger-motivated food acquisition.     

Complex attributes of lateral hypothalamic neurons in the regulation of feeding of alert rhesus monkeys

To elucidate the roles of glucose-sensitive (GS) and glucose-insensitive (GIS) cells of the lateral hypothalamic area (LHA), single neuron activity was recorded during 1) microelectrophoretic administration of chemicals, 2) a conditioned bar press feeding task, 3) gustatory, 4) olfactory, and 5) electrical brain stimulation. GS and GIS neurons showed different firing rate changes during phases of the task, and the responses were highly influenced by the palatability of the food and the motivational (hunger or satiety) state of the animal. The two groups of cells also differed in their responsiveness to gustatory and olfactory stimuli: GS neurons were more likely to respond to tastes and odors than GIS cells. Taste- and odor-responsive GS neurons were primarily suppressed by electrophoretically applied noradrenaline and were localized ventromedially within the LHA. The chemosensitive GIS cells, being organized along a dorsolateral axis, were especially excited by dopamine. The two sets of neurons had distinct connections with associative (orbitofrontal, prefrontal) cortical areas. GS and GIS cells, thus, appear to have differential and complex attributes in the control of feeding.     

Functional heterogeneity of the monkey lateral hypothalamus in the control of feeding

Regional differences in the effects of electrical (ES) and chemical stimulation on execution of a bar-press feeding task, and in neuronal activity related to feeding, glucose sensitivity, and odor responsiveness were examined in the lateral hypothalamic area (LHA) of monkeys. In satiated animals, ES of the far lateral and ventral LHA induced bar-press feeding. In hungry animals, ES of the dorsal LHA suppressed the feeding task only during the stimulation period, but prolonged feeding suppression that occurred after ES of the ventromedial LHA. Microinjection of Na-glutamate into LHA sites where ES was effective in suppressing feeding had no effect, but it was effective in the medial hypothalamus. Glucose-sensitive (GS) neurons decreased in activity during bar pressing and/or during the ingestion period. Glucose-insensitive (GIS) neurons showed a cue-related excitation more often than GS neurons. Odor-responding GS and GIS cells were localized in ventromedial and lateral LHA sites, respectively. The present study suggests the regional heterogeneity of the LHA in feeding regulation, depending on both hunger and satiety states.     

Visual responses related to food discrimination in monkey lateral hypothalamus during operant feeding behavior

Single neuron activity was recorded from monkey lateral hypothalamic area (LHA) to relate neuronal events to food discrimination and initiation of procurement movement in operant bar press feeding behavior. Of 429 neurons tested, 68 (16%) responded during visual phase. Of these, 30 (7%) responded selectively to the sight of food or non-food associated with a juice reward, but not to the sight of meaningless non-food or food associated with aversive saline. Neuronal activity related to discrimination was readily influenced by extinction, reversal or satiation. The strength of visual responses was correlated with latency of bar press initiation and speed of bar pressing, but was not related directly to bar press movement. These suggest that the LHA is deeply involved in discrimination of reinforcement or non-reinforcement, and might be associated with higher functions to regulate internal states such as physiological need to get food during operant feeding behavior.     

Movement and non-movement related pallidal unit activity during bar press feeding behavior in the monkey

Activity was recorded from 358 neurons in the globus pallidus (GP) of monkeys (Macaca fuscata) during an operant feeding task consisting of 3 stages: (1) food or non-food presentation (1st stage); (2) bar pressing (2nd stage); and (3) food acquisition and ingestion (3rd stage). There were two kinds of neurons, one with high and the other with very low (almost silent), spontaneous firing rates. Two hundred and four neurons (57%) responded in one or more of the feeding stages. Of the 21 neurons which responded in the 1st stage, two responded selectively to food presentation, and 19 responded to both food and non-food visual presentation. One hundred and seventy-four neurons (49%) and 107 neurons (30%) responded in the 2nd and 3rd stages, respectively, and 106 (30%) of these were directly related to specific feeding motor acts such as arm extension, flexion, bar pressing, grasping, chewing etc. Both high and low firing neurons responded to motor acts with sharp or gradual onset. More than half of those that responded to arm extension showed laterality (contra or ipsi)- and function (extension or flexion)-dependent responses. The incidence of the motor related neurons was higher in the caudodorsal part of the GP. On the other hand, about one third, especially in the rostroventral part of the GP, showed dissociating responses in that they responded during bar pressing for food or during ingestion in an operant task, but not during bar pressing for non-food or during forcible ingestion. The magnitude of firing changes during arm extension and bar pressing depended on the nature of the food. Moreover, in trials using new food or false (model) food, firing changes during bar press appeared or disappeared within a few trials with no correlation to bar press movement. These data suggest heterogeneous functions within the GP; the caudodorsal part is strictly concerned with motor execution and preparation, while the rostroventral part is not related to motor function directly, but may rather be important in coupling internal, motivational information to the motor system.     

Learning and integration of rewarding and aversive stimuli in the rat lateral hypothalamus

Single neuron activity was recorded in the lateral hypothalamus (LHA) and lateral preoptic-anterior hypothalamic area (IPOA-AHA) of the rat during discrimination learning of cue tones that predicted glucose or intracranial self-stimulation as rewarding stimuli, or electric shock or tail pinch as aversive stimuli, using identical behavior, licking. Rewarding and aversive stimuli had opposite effects on the same LHA neurons, but had the same effects on IPOA-AHA neurons. Neurons in the LHA that differentiated between reward and aversion acquired discrimination of the respective cue tones, while IPOA-AHA neurons responded in the same way to cue tones whether they preceded reward or aversion. The results suggest reward- and aversion-related integrative functions in the LHA and arousal or attentional functions in the IPOA-AHA.     

Influence of acetylcholine on neuronal activity of monkey amygdala during bar press feeding behavior

Single neuron activity in the monkey amygdala was investigated during cue signalled conditioned bar press feeding behavior and the effects of electrophoretically applied acetylcholine (ACh) and atropine were analyzed. ACh increased the firing rate of one third of the neurons tested; these excitatory responses were inhibited by the muscarinic receptor antagonist atropine. No characteristic location of ACh-sensitive neurons was found, cells were diffusely distributed throughout the amygdala. Activity of ACh-sensitive neurons did not correlate with any particular event during the bar press feeding task. However, continuous application of ACh at low current intensity during the task significantly enhanced the task-related excitatory firing patterns, or markedly attenuated the inhibitory responses. Continuous application of atropine elicited or enhanced inhibitory response patterns. These results suggest that the cholinergic system of the monkey amygdala facilitates neuronal excitation but attenuates inhibition related to various phases of feeding behavior, such as to cue recognition, food aquisition and rewarding process.     

Neuronal activity in the medial orbitofrontal cortex of the behaving monkey: Modulation by glucose and satiety

To investigate neuronal responses to interoceptive information, single neuron activity of the orbitofrontal cortex (OBF) of the behaving monkey was recorded during glucose injection, natural feeding and an operant bar press feeding task. Intravenous glucose injection had almost no effect on rates of spontaneous firing, but tended to attenuate neuronal responses during the bar press and reward periods. In about half of the neurons tested, the spontaneous firing rate changed for a relatively long period after the animal ate to satiety. The results suggest that blood glucose concentration is a modulatory factor in neuronal processing for feeding, but other interoceptive information generated by satiety strongly affects the activity of OBF neurons.     

Role of bar press-related neurons in the dorsolateral prefrontal cortex during task performance by monkey

Extracellular single neuron activity of the dorsolateral prefrontal cortex (DL) was recorded in the monkey, during bar pressing for reward. The bar press-related neurons which exhibited excitation or inhibition during the bar press period were found to be scattered diffusely in the DL. Activity changes that arose during the bar press period also appeared when the experimenter pressed the bar for the monkey. When delivery of food was delayed for a random time after cue tone on, bar press responses were still confined to the bar press period and did not extend beyond the cue tone. These results, together with the lesion studies, suggest that bar press-related neurons are involved in the animal's concentration during the bar press period.     

Neuronal responses in monkey lateral hypothalamus during operant feeding behavior

Single neuron activity was recorded from monkey lateral hypothalamus to investigate neuronal events correlated with operant bar press feeding behavior. The behavioral paradigm was divided into three phase: visual (discrimination), bar press (procurement), and ingestion (consummatory). Of 669 neurons tested, 158 (24%) responded in one or more phases. During the visual phase, 106 neurons (16%) responded. Of 80 neurons that responded in the visual phase and were tested systematically, 33 (41%, 33/80) responded selectively to the sight of food or nonfood objects associated with a juice reward, but not to the sight of nonfood or objects associated with aversive saline. Neuronal activity related to discrimination was modulated by satiation and learning (i.e., acquisition and extinction). During the bar press phase, 51 neurons (7.6%) responded. These responded tonically during the early or late stage of the bar press period, but did not depend on individual bar pressing motions. During ingestion, 90 neurons (13%) responded. The ingestion response was modulated by palatability of food and satiation. Data suggest that the LHA is deeply involved in operant feeding behavior; discrimination of food, drive to get food, and perception of reward, all of which are affected by learning and internal states such as hunger and satiety.     

Functional role of the limbic system and basal ganglia in motivated behaviors

It has been suggested that the cortico- and limbic-striatal systems are important in various motor functions such as motivated behaviors. In this paper we review our previous studies to investigate neuronal mechanisms of feeding behaviors. We recorded neuronal activity from the amygdala, caudate nucleus, globus pallidus, and substantia nigra during feeding behavior in monkeys, and compared neuronal responses recorded from these brain areas. First, of 710 amygdalar neurons tested, 129 (18.2%) responded to single sensory stimulation (48 to vision, 32 to audition, 49 to ingestion), 142 (20%) to multimodal stimulation, and 20 to only one item with affective significance. Eight food related amygdalar neurons were tested in reversal by salting food or introducing saline, and all responses were modulated by reversal. These results suggest that the amygdala might be important in ongoing recognition of the affective significance of complex stimuli (food-nonfood discrimination).

Second, activity was recorded from 351 neurons in the head of the caudate nucleus of monkeys during an operant feeding task. The 16% of these neurons responded in the discrimination phase. Some of these neurons responded specifically to food. The magnitude of these food-specific neurons depend on the rewarding nature of the food (reward value), and was inversely related to the latency of the onset of bar press. Of the caudate neurons, 10% responded in the bar press phase. Activity of most neurons which responded in the bar press phase was not correlated to individual bar presses. Cooling of the dorsolateral prefrontal cortex abolished sustained responses during bar pressing, but did not abolish the feeding behavior. However, bar press speed tended to be delayed by prefrontal cooling.

Third, activity of 358 neurons was recorded from the monkey globus pallidus, and 204 neurons responded during the feeding task. In the globus pallidus, few neurons responded to food in the discrimination phase. On the other hand, activity of most responsive neurons changed during bar press and/or ingestion phases. Activity of about half of these responsive neurons was directly related to specific feeding motor acts such as arm extension, flexion, bar pressing, grasping, chewing, etc. Some of these neurons showed motor-related responses with gradual and preparatory responses. These motor-related neurons were located mainly in the caudodorsal part of the globus pallidus. On the other hand, about one third, especially in the rostroventral part of the globus pallidus, showed dissociating responses in that they responded during bar pressing for food or during ingestion in an operant task, but not during bar pressing for nonfood or during forcible ingestion. The response magnitude of the neurons during arm extension and bar pressing depended on the nature of the food.

Fourth, activity of 261 neurons was recorded from the substantia nigra pars reticulata. Most of responding neurons (more than two-thirds of the recorded neurons) responded during the bar press and/or ingestion phases. Activity of the one-third of neurons was related to specific motor execution such as arm extension, flexion and bar pressing, but not to motor preparation. These neurons were located mainly in the rostral part of the nucleus. More than one-third of the recorded neurons responded during feed and/or drinking acts and intra- and perioral sensory stimuli, and were located mainly in the caudomedial part of the nucleus.

Based upon these responses and known anatomical evidence, various information including that from the amygdala and prefrontal cortex is integrated in the basal ganglia, and converted to coordinated motivated behaviors such as feeding behavior.

     

Response properties of lateral hypothalamic neurons during ingestive behavior with special reference to licking of various taste solutions

Activity of 58 single neurons in the lateral hypothalamic area (LHA) was recorded while Wistar male rats were drinking water and various taste solutions in a test box. A cue tone was presented before opening of a shutter for access to a drinking spout. Except 8 neurons which were non-responsive in the present experimental paradigm, 50 neurons were classified into 3 types according to their response properties: (1) 10 neurons changed their activity with arousal state or circadian rhythm, (2) 10 neurons responded to specific sensory stimuli, i.e. 2 were classified as taste-responsive neurons, which responded excitatory to sodium salts, 3 neurons responded to olfactory stimulation, 5 to somatosensory stimulation applied to the perioral region, and (3) the remaining 30 decreased their activity during licking of liquids regardless of their qualities. Besides this classification, activity of 28 of 58 LHA neurons was altered after onset of the cue tone (or before start of licking), i.e. 24 increased their activity (learned anticipatory response), and 3 modulated their tonic activity into burst discharges corresponding to sniffing, and 1 increased its activity in relation to stepping toward the drinking spout. These data suggest that about half of the LHA neurons increased their activity in anticipatory (searching or approaching) periods just before ingestion, and decreased activity in rewarding periods during ingestion of water or sapid solutions.     

Dopamine and ACH involvement in plastic learning by hypothalamic neurons in rats

Unit activity in the rat lateral hypothalamus (LHA) was recorded during discrimination learning of cue tone stimuli (CTS). CTS+ predicted reward (glucose or intracranial self-stimulation); CTS- predicted aversion (electric shock or tail pinch); and all behavior responses were by the same act, licking. Roles of the LHA dopaminergic and cholinergic systems in CTS learning were investigated by electrophoretic application of dopamine (DA) and acetylcholine (ACh), and their antagonists. The CTS+, the predicted reward and DA, all had similar effects (inhibition) on many LHA neurons; and these were all opposite to the effects (excitation) of CTS-, the predicted aversion, and ACh. Neural responses to CTS+ were blocked by spiperone, and responses to CTS- were blocked by atropine. Sensitivity of LHA neurons to DA was reduced by extinction of CTS+ learning for reward, and sensitivity to ACh was reduced by CTS- learning for aversion. The data suggest that afferent DA and ACh inputs to LHA neurons are essential for plastic CTS+ and CTS- learning.     

Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus

The activity of 394 neurons in the head of the caudate nucleus and the most anterior part of the putamen was analyzed in 3 behaving rhesus monkeys in order to analyze the functions of this part of the striatum. Of these neurons, 64.2% responded in the tests used in relation to, for example, environmental events, movements made by the monkey, the performance of a visual discrimination, or during feeding. However, only relatively small proportions of these neurons had responses which were unconditionally related to visual (9.6%), auditory (3.5%), or gustatory (0.5%) stimuli, or to movements (4.1%). Instead, the majority of the responsive neurons had activity in relation to stimuli or movements which was conditional, in that the responses occurred in only some test situations, and were often dependent on the performance of a task by the monkeys. Thus, it was found in the visual discrimination task that 14.5% of the neurons responded during a 0.5 sec tone/light cue period which signalled the start of each trial; 31.1% responded in the period in which the discriminative visual stimuli were shown, with 24.3% of these responding more to either the visual stimulus which signified food reward or to that which signified punishment; and 6.2% responded in relation to lick responses. Yet these neurons typically did not respond in relation to the cue stimuli, to the visual stimuli, or to movements, when these occurred independently of the task, or when performance of the task was prevented. Comparably, of the neurons tested during feeding, 25.8% responded when the food was seen by the monkey, 6.2% when he tasted it, and 22.4% during a cue given by the experimenter that a food or non-food object was about to be presented. However, only few of these neurons had responses to the same stimuli presented in different situations.It is concluded that many neurons in the head of the caudate nucleus and the most anterior part of the putamen respond in relation to events which are used as cues to prepare for the performance of tasks, including feeding, in which movements must be initiated. Other neurons respond in relation to the stimuli used and the movements made in these tasks. However, the majority of these neurons do not have unconditional sensory or motor responses. It is therefore suggested that the anterior neostriatum contains neuronal mechanisms which are important in the process by which environmental cues are used in the preparation of behavioral responses, and in the initiation of particular behavioral responses made in particular situations to particular environmental stimuli. Deficits in the initiation of movements following damage to striatal pathways may arise in part because of interference with these functions of the anterior neostriatum.     

Characteristics of rat lateral hypothalamic neuron responses to smell and taste in emotional behavior

Single unit activity in the lateral hypothalamus (LHA) of the rat was recorded while the animal learned to discriminate cue signals. Normally preferred potables (glucose, orange, or grape solution) or intracranial self-stimulation (ICSS) were used as rewards. Electric shock or tail pinch were used as aversive stimuli. The same behavior, licking, was the response required to either obtain the rewarding stimuli or avoid the aversive ones. For positive reinforcement a rat was rewarded with fluid or ICSS upon licking a spout presented in front of its mouth. In negative reinforcement experiments, an aversive stimulus, electric shock or tail pinch, was applied if the rat did not lick the spout. Solutions having smell only, taste only, or smell-plus-taste, were prepared from oranges or grape extract. Of 392 neurons analyzed, 256 responded differentially to rewarding and aversive stimuli, and 138 of these were tested with the 3 different solutions. Similar LHA neural responses occurred during actual drinking of the 3 kinds of solutions, as well as on recognition of the cue signal. Responses to smell only had shorter latency than responses to taste only. Neural activity in response to solutions that could be both smelled and tasted was the sum of activity in response to taste-only solutions plus that in response to smell-only solutions. Cue signal responses were rapidly acquired, usually within 2-5 trials, for both taste-only and smell-only solutions. The results indicate the integration of both taste and olfactory information by the same LHA neurons, and these neurons are involved in cue signal learning. Present results of LHA neuronal responses to taste and smell suggest that the intensity of gustation and olfaction may add together to enhance instinctive hedonic sensations. These neurons are involved in the formation of stimulus-reinforcement association in learning, and in elicitation of conditioned emotional responses.     

Central action of endogenous sugar acid (2-buten-4-olide): comparison with local anesthesia in hypothalamus

Rats were trained to discriminate cue tone stimuli (CTS) predicting reward (CTS+) [juice or intracranial self-stimulation (ICSS)], or aversion (CTS-) (mild electric shock or tail pinch). Unit activity in the lateal hypothalamus (LHA) and lateral preoptic-anterior hypothalamic area (lPOA-AHA) of the rat was recorded during CTS learning. The effects of local anesthesia of the amygdala (AM), ventral tegmental area (VTA) or LHA by procaine hydrochloride, and the effects of intraperitoneal or intravenous 2-buten-4-olide (2-B4O) on LHA neural activity and licking behavior were compared. LHA neurons differentiated between rewarding and aversive stimuli, and acquired corresponding discrimination of CTS+ and CTS-. In the lPOA-AHA, neurons responded similarly to CTS+, rewarding stimuli, CTS- and aversive stimuli. Procainization of the AM suppressed LHA neural responses to CTS1+ predicting juice, and stopped licking for juice. Procainization of the VTA suppressed LHA neural responses to CTS2+ predicting ICSS, and stopped licking for ICSS. LHA procainization suppressed both licking for juice and ICSS. Both intraperitoneal and intravenous 2-B4O stopped licking for juice and ICSS, but did not influence LHA responses to CTS1+ or CTS2+. The results suggest that dynamic interaction of AM-LHA-VTA are important for CTS+ learning, and 2-B4O acts directly on LHA neurons while maintaining afferent sensory inputs to the LHA.     

Caudate unit activity during operant feeding behavior in monkeys and modulation by cooling prefrontal cortex

Activity was recorded from 351 neurons in the head of the caudate nucleus (CD) of monkeys during an operant feeding task consisting of: (1) food or non-food presentation (P); (2) bar pressing (B); and (3) food acquisition and ingestion (I). Of 45 neurons which responded in the P phase and were tested systematically, 27 responded to visual presentation of both food and non-food (non-specific response), and 18 responded to food presentation only (food specific response). The magnitude of food specific responses depended on the nature of the food and was inversely related to the latency of the onset of bar pressing. Thirty-five neurons responded in the B phase: 28 changed firing rate continuously with no correlation to individual bar presses, while the activity of the other 7 was related to each bar press. In the I phase, 62 neurons responded to separate events: the activity of more than half (39 neurons) was often related to chewing movement or gustatory stimuli, and that of one third (23 neurons) changed during individual arm movements. The neurons which responded in the P phase were found to be distributed widely in the head of the CD except for its central zone, while the neurons which responded in the I phase were in the medial part. Cooling of the dorsolateral prefrontal cortex abolished the continuous responses seen in the B phase, but did not abolish the feeding behavior. The data suggest that in the head of the CD there are several groups of neurons that have different functions and different distributions: food specific, sensory integration responses, non-motor responses driven by the frontal cortex, motor responses coupled to various movements, and sensory responses which apparently originate in the intra-oral cavity. These functions may arise sequentially, or in correspondence with integration of the sensory and motor systems to produce coordinated behavior.     

Hippocampal neuronal responses during signaled licking of gustatory stimuli in different contexts

Neuroanatomical studies suggest that hippocampal formation (HF) receives information from all sensory modalities including taste via the parahippocampal cortices. To date, however, no neurophysiological study has reported that HF neurons encode taste information. In the present study, we recorded CA1 HF neurons from freely behaving rats during performance of a visually‐guided licking task in two different triangular chambers. When a cue lamp came on, the rats were required to press a bar to trigger a tube to protrude into the chambers for 3 s. During this period, the rats could lick one of six sapid solutions: [0.1M NaCl (salty), 0.3M sucrose (sweet), 0.01M citric acid (sour), 0.0001M quinine HCl (bitter), 0.01M monosodium L ‐glutamate (MSG, umami), and a mixture of MSG and 0.001M disodium‐5′‐inosinate (IMP) (MSG+IMP)], and distilled water. Of a total 285 pyramidal and interneurons, the activity of 173 was correlated with at least one of the events in the task—illumination of cue lamps, bar pressing, or licking the solution. Of these, 137 neurons responded during licking, and responses of 62 of these cells were greater to sapid solutions than to water (taste neurons). Multivariate analyses of the taste neurons suggested that, in the HF, taste quality might be encoded based on hedonic value. Furthermore, the activity of most taste neurons was chamber‐specific. These results implicate the HF in guiding appetitive behaviors such as conditioned place preference. © 2010 Wiley‐Liss, Inc.