The cingulate gyrus is a major part of the "anatomical limbic system" and, according to classic accounts, is involved in emotion. This view is oversimplified in light of recent clinical and experimental findings that cingulate cortex participates not only in emotion but also in sensory, motor, and cognitive processes. Anterior cingulate cortex, consisting of areas 25 and 24, has been implicated in visceromotor, skeletomotor, and endocrine outflow. These processes include responses to painful stimuli, maternal behavior, vocalization, and attention to action. Since all of these activities have an affective component, it is likely that connections with the amygdala are critical for them. In contrast, posterior cingulate cortex, consisting of areas 29, 30, 23, and 31, contains neurons that monitor eye movements and respond to sensory stimuli. Ablation studies suggest that this region is involved in spatial orientation and memory. It is likely that connections between posterior cingulate and parahippocampal cortices contribute to these processes. We conclude that there is a fundamental dichotomy between the functions of anterior and posterior cingulate cortices. The anterior cortex subserves primarily executive functions related to the emotional control of visceral, skeletal, and endocrine outflow. The posterior cortex subserves evaluative functions such as monitoring sensory events and the organism's own behavior in the service of spatial orientation and memory.
We have examined the origin and topography of cortical projections to area PO, an extrastriate visual area located in the parieto-occipital sulcus of the macaque. Distinguishable retrograde fluorescent tracers were injected into area PO at separate retinotopic loci identified by single-neuron recording. The results indicate that area PO receives retinotopically organized inputs from visual areas V1, V2, V3, V4, and MT. In each of these areas the projection to PO arises from the representation of the periphery of the visual field. This finding is consistent with neurophysiological data indicating that the representation of the periphery is emphasized in PO. Additional projections arise from area MST, the frontal eye fields, and several divisions of parietal cortex, including four zones within the intraparietal sulcus and a region on the medial dorsal surface of the hemisphere (MDP). On the basis of the laminar distribution of labeled cells we conclude that area PO receives an ascending input from V1, V2, and V3 and receives descending or lateral inputs from all other areas. Thus, area PO is at approximately the same level in the hierarchy of visual areas as areas V4 and MT. Area PO is connected both directly and indirectly, via MT and MST, to parietal cortex. Within parietal cortex, area PO is linked to particular regions of the intraparietal sulcus including VIP and LIP and two newly recognized zones termed here MIP and PIP. The wealth of connections with parietal cortex suggests that area PO provides a relatively direct route over which information concerning the visual field periphery can be transmitted from striate and prestriate cortex to parietal cortex. In contrast, area PO has few links with areas projecting to inferior temporal cortex. The pattern of connections revealed in this study is consistent with the view that area PO is primarily involved in visuospatial functioning.
In several areas of the macaque brain, neurons fire during delayed-response tasks at a rate determined by the value of the reward expected at the end of the trial. The activity of these neurons might be related to the value of the expected reward or to the degree of motivation induced by expectation of the reward. We describe results indicating that the nature of reward-dependent activity varies across areas. Neuronal activity in orbitofrontal cortex represents the value of the expected reward, whereas neuronal activity in premotor cortex reflects the degree of motivation.
One of the most fundamental functions of the brain is to predict upcoming events on the basis of the recent past. A closely related function is to signal when a prediction has been violated. The identity of the brain regions that mediate these functions is not known. We set out to determine whether they are implemented at the level of single neurons in the visual system. We gave monkeys prolonged exposure to pairs of images presented in fixed sequence so that each leading image became a strong predictor for the corresponding trailing image. We then monitored the responses of neurons in the inferotemporal cortex to image sequences that obeyed or violated the transitional rules imposed during training. Inferotemporal neurons exhibited a transitional surprise effect, responding much more strongly to unpredicted transitions than to predicted transitions. Thus, neurons even in the visual system make experience-based predictions and react when they fail.macaque | vision | plasticity T he inferotemporal cortex (ITC), the terminus of the ventral stream of visual areas (1), plays a critical role in object vision (2, 3). ITC neurons respond with individual patterns of selectivity to complex images (4). Training monkeys to discriminate between images (5-7), categorize them (8, 9), or form associations between them (10-12) induces functional changes among neurons in the ITC which have the effect of strengthening the representation of image attributes relevant to task performance. Even passive viewing causes changes in neuronal visual responsiveness. Repeated viewing of a single image leads to a weakening of responses to it (13,14). Repeated viewing of two images close together in time leads to pair coding: a tendency for neurons responsive to one image also to respond to the other (15-17). The effects of passive viewing, because they do not depend on task demands, fall into the category of unsupervised statistical learning.An important form of unsupervised learning not previously studied at the level of single neurons concerns transitional statistics. The learning of transitional statistics has been the focus of much behavioral study in humans because it is thought to underlie the development during infancy of the ability to perceive event boundaries including word boundaries in speech (18,19). Human infants passively exposed to a stimulus stream in which certain visual images always follow certain others automatically register the transitional rules as evidenced by their orienting preferentially to a test stream containing novel transitions (20). The adult human brain is sensitive to transitional probabilities, as evidenced by its generating strong responses to improbable transitions at the level of scalp potential and blood oxygenation measures (21-27). Monkeys, like human infants, have been reported to learn transitional probabilities and to orient preferentially to improbable transitions (28). No effort has been made as yet to characterize the underlying neuronal mechanisms (29). We hypothesized that neurons in the ITC ...
In several regions of the macaque brain, neurons fire during delayed response tasks at a rate determined by the value of the reward expected at the end of the trial. The activity of these neurons might be related either to the internal representation of the appetitive value of the expected reward or to motivation-dependent variations in the monkey's level of motor preparation or motor output. According to the first interpretation, reward-related activity should be most prominent in areas affiliated with the limbic system. According to the second interpretation, it should be most prominent in areas affiliated with the motor system. To distinguish between these alternatives, we carried out single-neuron recording while monkeys performed a memory-guided saccade task in which a visual cue presented early in each trial indicated whether the reward would be large or small. Neuronal activity accompanying task performance was monitored in the dorsolateral prefrontal cortex (PFC), the frontal eye field (FEF), a transitional zone caudal to the frontal eye field (FEF/PM), premotor cortex (PM), the supplementary eye field (SEF), and the rostral part of the supplementary motor area (SMAr). The tendency for neuronal activity to increase after cues that predicted a large reward became progressively stronger in progressively more posterior areas both in the lateral sector of the frontal lobe (PFC < FEF < FEF/PM < PM) and in the medial sector (SEF < SMAr). The very strong reward-related activity of premotor neurons was presumably attributable to the monkey's motivation-dependent level of motor preparation or motor output. This finding points to the need to determine whether reward-related activity in other nonlimbic brain areas, including dorsolateral prefrontal cortex and the dorsal striatum, genuinely represents the value of the expected reward or, alternatively, is related to motivational modulation of motor signals.
Visual object recognition is thought to depend on experienceinduced changes in inferotemporal (IT) cortex, such that neurons become more selective for (or more responsive to) learned images [1][2][3][4] . This view is consistent with evidence showing that lesions in IT interfere with pattern recognition 5,6 , that neurons in IT are pattern-selective 5,6 and that IT is a site of experience-dependent plasticity. Plasticity has been shown in IT by the use of three approaches: (i) repeated exposure to a stimulus over a short period of time leads to a decline in response strength 7-10 , (ii) prolonged training on a visual paired associate task results in the emergence of neurons that are responsive to both members of the pair [11][12][13] and (iii) discrimination training. Training monkeys to discriminate among images is thought to induce changes in the strength and selectivity of neuronal responses to those images, but studies to date have produced contradictory and inconclusive results. On the one hand, some neurons seem to become markedly selective for learned images. For example, in a study of monkeys trained to discriminate among wire objects 14,15 , several units showed "a remarkable selectivity" for individual views that the monkey had learned to recognize. On the other hand, two studies involving a single day 16 or several months 17 of training do not show evidence of enhanced selectivity for images in the training set. In another study 18 , discrimination training resulted in a subtle enhancement of stimulus selectivity at the population level, but this effect was shown by comparing trained to untrained monkeys rather than by comparing responses to learned and unlearned stimuli in the same monkey. Thus, innate differences between monkeys may have contributed to the result. Finally, learned images have been reported to elicit higher firing rates than unlearned images [18][19][20] . Here we investigated the impact of visual discrimination training on neuronal responses to parts of images and to whole images in inferotemporal (IT) cortex. Monkeys were trained to discriminate among 'baton' stimuli consisting of discrete top and bottom parts joined by a vertical stem. With separate features at each end, we were able to manipulate the two parts of each baton independently. After training the monkeys, we used single-cell recording to compare neuronal responses to learned and unlearned batons. Responses to learned batons, though not enhanced in strength, were enhanced in selectivity for both individual parts and for whole batons. Whole-baton selectivity arose from a form of conjunctive encoding whereby two parts together exerted a greater influence on neuronal activity than predicted by the additive influence of each part considered individually. These results indicate a possible neural mechanism for holistic or configural effects in expert versus novice observers.An important question not addressed in previous studies is whether discrimination training enhances neuronal selectivity for whole images or for the parts...
The claustrum is a telencephalic cell group (Fig. 1A, B) possessing widespread reciprocal connections with the neocortex. In this regard, it bears a unique and striking resemblance to the thalamus. We have now examined the anatomical ordering of pathways linking the claustrum with sensory areas of the cat neocortex and, in parallel electrophysiological experiments, have studied the functional organization of claustral sensory zones so identified. Our findings indicate that there are discrete visual and somatosensory subdivisions in the claustrum interconnected with the corresponding primary sensory areas of the neocortex and that the respective zones contain orderly retinotopic and somatotopic maps. A third claustral region receiving fibre projections from the auditory cortex in or near area Ep was found to contain neurones responsive to auditory stimulation. We conclude that loops connecting sensory areas of the neocortex with satellite zones in the claustrum contribute to the early processing of exteroceptive information by the forebrain.
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