Monkey hippocampal neuron responses to complex sensory stimulation during object discrimination.

The purpose of this study was to investigate, during the performance of an object discrimination task, responses of neurons in the monkey hippocampal formation to the sight of several objects that have biological meaning, and compare these responses with those of amygdalar neurons studied previously using the same task. Neuronal activity in the hippocampal formation of conscious monkeys was recorded during performance of a task that led to presentation of familiar rewarding, familiar aversive, or unfamiliar objects. Of 864 neurons recorded in the hippocampal formation and adjacent cortices, 160 (18.5%) responded to the sight of a certain object(s). Responses to the sight of different kinds of objects were analyzed in detail. Nondifferential neurons (n = 73) responded to different objects with no significant difference in response magnitudes, and differential neurons (n = 87) responded to different objects with different response magnitudes. Of the differential neurons, 23 responded more strongly to rewarding objects than to other objects (rewarding-object-dominant neurons), but the magnitude of responses to objects did not necessarily correlates with the order of preferences to the objects as determined from observation of animal behavior. Aversive-object-dominant neurons (n = 13) responded more to aversive objects than to other objects. Unfamiliar-object-dominant neurons (n = 7) responded more to unfamiliar objects than to familiar objects. Selective neurons (n = 10) responded selectively to only one object or one category of objects. Fourteen of the rewarding- or averse-object-dominant neurons were tested in extinction or reversal trials. In 12 of 14 neurons, responses to a rewarding or aversive object did not change, or slightly weakened, in extinction or reversal trials. The results suggest the following. (1) Responses of rewarding- or aversive-object-dominant neurons may be involved in object-reward or object-aversion association. However, responses of many of these neurons might reflect past inputs to reinforcement rather than extant emotional processing. (2) Responses of unfamiliar-object-dominant neurons may be involved in recognition of objects based on their familiar or unfamiliar aspects. These results are further discussed and compared with responsiveness of amygdalar neurons.     

Visual responses of neurons in the dorsolateral amygdala of the alert monkey

There is evidence that the inferotemporal visual cortex in the monkey projects to the amygdala, and evidence that damage to this region impairs the learning of associations between visual stimuli and reward or punishment. In recordings made in the amygdala to determine whether or not visual responses were found, and if so how they were affected by the significance of the visual stimuli, neurons were found in the dorsolateral part of the amygdala with visual responses which in most cases were sustained while the animal looked at effective visual stimuli. The latency of the responses was 100 to 140 ms or more. The majority (85%) of these neurons responded more strongly to some stimuli than to others, but physical factors which accounted for the responses of the neurons, such as shape, size, orientation, color, or texture, could not usually be identified. Although 22 (19.5%) of these neurons responded primarily to food objects, the responses were not uniquely food-related. Furthermore, although some neurons responded in a visual discrimination test to a visual stimulus which indicated reward, and not to a visual stimulus which indicated saline, only minor modifications of the magnitude of the neuronal responses to the stimuli were obtained when the reward-related significance of the stimuli was reversed. The visual responses of these amygdaloid neurons were thus intermediate in some respects between those of neurons in the inferotemporal cortex, which are not affected by the significance of visual stimuli, and those of neurons in a region to which the amygdala projects, the lateral hypothalamus and substantia innominata, where neurons respond to visual stimuli associated with food reward.     

Sex-specific developmental changes in amygdala responses to affective faces

It is hypothesized that adolescent development involves a redistribution of cerebral functions from lower subcortical structures to higher regions of the prefrontal cortex to provide greater self-control over emotional behavior. We further hypothesized that this redistribution is likely to be moderated by sex-specific hormonal changes. To examine developmental sex differences in affective processing, 19 children and adolescents underwent fMRI while viewing photographs of faces expressing fear. Males and females differed in the pattern of their amygdala vs prefrontal activation during adolescent maturation. With age, females showed a progressive increase in prefrontal relative to amygdala activation in the left hemisphere, whereas males failed to show a significant age related difference. There appear to be sex differences in the functional maturation of affect-related prefrontal-amygdala circuits during adolescence.     

Neurons in the amygdala of the monkey with responses selective for faces

To investigate the functions of the amygdala in visual information processing and in emotional and social responses, recordings were made from single neurons in the amygdala of the monkey. A population of neurons (40 of more than 1000 recorded in 4 monkeys) was investigated which responded primarily to faces. These neurons typically (1) responded to some human or monkey faces, which were presented to the monkey through a large aperture shutter so that response latencies could be measured, or were simply shown to the monkey, (2) responded to 2-dimensional representations of these faces, as well as to real 3-dimensional faces, (3) had no responses or only small (less than half maximum) responses to gratings, simple geometrical, other complex 3-D stimuli, or to arousing and aversive stimuli, (4) had response latencies of 110-200 ms, (5) were located in the basal accessory nucleus of the amygdala, (6) responded differently to different faces, as shown by measures of d', and could thus over a population of such neurons code information useful for making different responses to different individuals, (7) could in some cases (9/11 tested) respond to parts of faces, and (8) in a few cases (4/19 tested) responded more to a face which produced an emotional response. A comparison made in three monkeys of the responses of these neurons with the responses of 77 neurons with face-selective responses recorded in the cortex of the superior temporal sulcus (STS) showed that the amygdaloid neurons had longer response latencies (110-200 compared to 90-140 ms), and were in some respects more selective in their responses to different faces. It is suggested that the deficits in social and emotional behavior produced by amygdala lesions could be due in part to damage to a neuronal system specialized in utilizing information from faces so that appropriate social and emotional responses can be made to different individuals.     

Single neuron activity in dorsolateral prefrontal cortex of monkey during operant behavior sustained by food reward

The activity of 190 neurons was recorded from the dorsolateral prefrontal cortex of monkeys during an operant task that consisted of 3 phases: visual discrimination of food and non-food, bar pressing to gain access to the food and ingestion. In area 8, a fairly large proportion of the 49 recorded neurons responded in both the visual discrimination (37%) and motor initiation (35%) phases. Some functional heterogeneity seems evident within area 8 since visual discrimination responses were rostral, visuokinesis was central and motor initiation was in the caudal bank of the arcuate sulcus. Neurons in area 9 responded primarily (37%) during the bar pressing phase and less during the visual discrimination phase. Neurons in area 10 responded variously during most phases of the task--food discrimination, bar pressing, and ingestion. Neurons in the periprincipal sulcal area usually responded in the visual discrimination phase, but some which did not respond to food presented in front of the subject responded to meaningful visual or auditory cues that were related to food reward. The data suggest that neurons in the dorsolateral prefrontal cortex have multiple functions related to all phases of complex, learned feeding behavior. Functional roles of the prefrontal cortex and the lateral hypothalamus in development of feeding behavior are discussed.     

Meditation-induced neuroplastic changes in amygdala activity during negative affective processing

Recent evidence suggests that the effects of meditation practice on affective processing and resilience have the potential to induce neuroplastic changes within the amygdala. Notably, literature speculates that meditation training may reduce amygdala activity during negative affective processing. Nonetheless, studies have thus far not verified this speculation. In this longitudinal study, participants (N = 21, 9 men) were trained in awareness-based compassion meditation (ABCM) or matched relaxation training. The effects of meditation training on amygdala activity were examined during passive viewing of affective and neutral stimuli in a non-meditative state. We found that the ABCM group exhibited significantly reduced anxiety and right amygdala activity during negative emotion processing than the relaxation group. Furthermore, ABCM participants who performed more compassion practice had stronger right amygdala activity reduction during negative emotion processing. The lower right amygdala activity after ABCM training may be associated with a general reduction in reactivity and distress. As all participants performed the emotion processing task in a non-meditative state, it appears likely that the changes in right amygdala activity are carried over from the meditation practice into the non-meditative state. These findings suggest that the distress-reducing effects of meditation practice on affective processing may transfer to ordinary states, which have important implications on stress management.     

Inactivation of basolateral amygdala specifically eliminates palatability-related information in cortical sensory responses

Evidence indirectly implicates the amygdala as the primary processor of emotional information used by cortex to drive appropriate behavioral responses to stimuli. Taste provides an ideal system with which to test this hypothesis directly, as neurons in both basolateral amygdala (BLA) and gustatory cortex (GC)-anatomically interconnected nodes of the gustatory system-code the emotional valence of taste stimuli (i.e., palatability), in firing rate responses that progress similarly through "epochs." The fact that palatability-related firing appears one epoch earlier in BLA than GC is broadly consistent with the hypothesis that such information may propagate from the former to the latter. Here, we provide evidence supporting this hypothesis, assaying taste responses in small GC single-neuron ensembles before, during, and after temporarily inactivating BLA in awake rats. BLA inactivation (BLAx) changed responses in 98% of taste-responsive GC neurons, altering the entirety of every taste response in many neurons. Most changes involved reductions in firing rate, but regardless of the direction of change, the effect of BLAx was epoch-specific: while firing rates were changed, the taste specificity of responses remained stable; information about taste palatability, however, which normally resides in the "Late" epoch, was reduced in magnitude across the entire GC sample and outright eliminated in most neurons. Only in the specific minority of neurons for which BLAx enhanced responses did palatability specificity survive undiminished. Our data therefore provide direct evidence that BLA is a necessary component of GC gustatory processing, and that cortical palatability processing in particular is, in part, a function of BLA activity.     

Cardiovascular responses to electrical stimulation of the amygdala in the rat

Cardiovascular responses to electrical stimulation of histologically verified sites in the amygdala were studied in rats. Stimulation of the basolateral and central nuclei elicited arterial hypotension in animals anesthetized with chloralose or urethan. Stimulation of the cortical nucleus resulted in no change in arterial pressure. With stimulation of the medial amygdala the arterial pressure response depended on the anesthetic; under chloralose hypotension was elicited and under urethan hypertension was elicited. In all animals stimulation of the amygdala did not elicit significant changes in heart rate or frequency of respiration. The cardiovascular responses were not altered by the administration of tubocurarine. The optimal parameters of stimulation were pulses of 2 msec duration at 80 Hz. It is suggested that the amygdala exerts complex modulatory influences in the control of the cardiovascular system and that its role will be understood by considering these fragmentary responses elicited in acute experimental conditions in relation to the cardiovascular changes observed in various natural behavioral states.     

Visual discrimination during reticular stimulation in the alert cat

The visual critical flicker frequency of cats was determined using a continuous testing procedure. Multiunit activity was recorded from the lateral geniculate nucleus and mesencephalic reticular formation during threshold determination. The effect on the visual thresholds of reticular stimulation was also studied. The data suggest that, in the alert animal, activation of the reticular formation facilitates motor rather than sensory functioning.     

Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey

The activity of single cells in the vestibular nuclei in alert, behaving monkey was studied by extracellular recording. A majority of the neurons found in the superior and the rostral medial vestibular nuclei can be divided into two classes on the basis of their discharge relationship to eye movements evoked during head rotation, visual target pursuit, or visual suppression of the vestibulo-ocular reflex. The firing rate of the first unit type is proportional to head rotational velocity (and the resulting compensatory eye velocity) but is not modulated during slow eye movements of pure visual origin. During visual suppression of the vestibulo-ocular reflex, the relationship of this type of unit discharge to head velocity remains unchanged, although the eye velocity is now zero. The second type of unit more closely resembles oculomotor neurons in that its discharge pattern is proportional to eye position and velocity during eye movements of both visual and vestibular origin. However during suppression of the vestibuloocular reflex this type of unit continues to show a greatly reduced but consistent modulation of discharge rate proportional to head velocity. Thus the direct projection of vestibular neurons to oculomotor neurons cannot by itself account for the ability of the monkey to completely suppress its vestibulo-ocular reflex.     

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

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 experiment was conducted a total of 14 times in two monkeys. The responses of individual neurons to the satiety stimuli were suppressed by as little as 1%, 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.     

Radiotelemetered activity from the amygdala during social interactions in the monkey.

Electrical activity from the amygdaloid nucleus in freely moving monkeys (Cercopithecus aethiops) during social interactions and alone were recorded via radiotelemetry. Spectral analysis of amygdaloid activity revealed highest power outputs occurred during behaviors related to sexual and aggressive interactions and the lowest with the tension-reducing behavior of grooming. Power output was not directly related to motor activity. These results suggest that amygdaloid activity is related to the emotional significance and degree of ambiguity of an interaction. It is hypothesized that at least two separate afferent systems, one for low frequencies and the other for fast frequencies, may be correlated with different behavioral events.     

Sequential onset of presynaptic molecules during olfactory sensory neuron maturation

Differentiated olfactory sensory neurons express specific presynaptic proteins, including enzymes involved in neurotransmitter transport and proteins involved in the trafficking and release of synaptic vesicles. Studying the regulation of these presynaptic proteins will help to elucidate the presynaptic differentiation process that ultimately leads to synapse formation. It has been postulated that the formation of a synapse between the axons of the sensory neurons and the dendrites of second order neurons in the olfactory bulb is a critical step in the processes of sensory neuron maturation. One approach to study the relationship between synaptogenesis and sensory neuron maturation is to examine the expression patterns of synaptic molecules through the olfactory neuron lineage. To this end we designed specific in situ hybridization probes to target messengers for proteins involved in presynaptic vesicle release. Our findings show that, as they mature, mouse olfactory neurons sequentially express specific presynaptic genes. Furthermore, the different patterns of expression of these presynaptic genes suggest the existence of discrete steps in presynaptic development: genes encoding proteins involved in scaffolding show an early onset of expression, whereas expression of genes encoding proteins involved in the regulation of vesicle release starts later. In particular, the signature molecule for glutamatergic neurons vesicle glutamate transporter 2 shows the latest onset of expression. In addition, contact with the targets in the olfactory bulb is not controlling presynaptic protein gene expression, suggesting that olfactory sensory neurons follow an intrinsic program of development. J. Comp. Neurol. 516:187–198, 2009. © 2009 Wiley‐Liss, Inc.     

Various responses of neurons of the caudate nucleus in alert cats to visual stimulation

Activity of sixty two neurons of the caudate nucleus to the visual stimuli were recorded in awake cats. It was found that most (52%) of tested neurons gave visual responses of sensory type evoked by the appearance of light stimulus in the visual field and only 11% of them were of the motor type related to the guided eye movement to the target. About a quarter of neurons responded to biologically significant objects revealing nonspecific responses. Several types of visual responses could be recorded from the same neuron. The data obtained permit supposing the presence of several parallel pathways for afferent visual influences on the caudate nucleus.     

Eye and head movements during vestibular stimulation in the alert rabbit

Rabbits passively oscillated in the horizontal plane with a free head tended to stabilize their head in space (re: earth-fixed surroundings) by moving the head on the trunk (neck angular deviation, NAD) opposite the passively imposed body rotation. The gain (NAD/body rotation) of head stabilization varied from 0.0 to 0.95 (nearly perfect stability) and was most commonly above 0.5. Horizontal eye movement (HEM) was inversely proportional to head-in-space stability, i.e. the gaze (sum of HEM, NAD, and body rotation) was stable in space (regardless of the gain of head stabilization). When the head was fixed to the rotating platform, attempted head movements (head torque) mimicked eye movements in both the slow and fast phases of vestibular nystagmus; tonic eye position was also accompanied by conjugate shifts in tonic head torque. Thus, while eye and head movements may at times be linked, that the slow eye and head movements vary inversely during vestibular stimulation with a free head indicates that the linkage is not rigid.Absence of a textured stationary visual field consistently produced a response termed ‘visual inattentiveness,’ which was characterized by, among other things, a reduction of head and gaze stability in space. This behavioral response could also be reproduced in a subject allowed vision during prolonged vestibular stimulation in the absence of other environmental stimuli. It is suggested that rabbits optimize gaze stability (re: stationary surroundings), with the head contributing variably, as long as the animal is attending to its surroundings.