The influence of vibrissal somatosensory processing in rat superior colliculus on prey capture.

The lateral part of intermediate layer of superior colliculus (SCl) is a critical substrate for successful predation by rats. Hunting-evoked expression of the activity marker Fos is concentrated in SCl while prey capture in rats with NMDA lesions in SCl is impaired. Particularly affected are rapid orienting and stereotyped sequences of actions associated with predation of fast moving prey. Such deficits are consistent with the view that the deep layers of SC are important for sensory guidance of movement. Although much of the relevant evidence involves visual control of movement, less is known about movement guidance by somatosensory input from vibrissae. Indeed, our impression is that prey contact with whiskers is a likely stimulus to trigger predation. Moreover, SCl receives whisker and orofacial somatosensory information directly from trigeminal complex, and indirectly from zona incerta, parvicelular reticular formation and somatosensory barrel cortex. To better understand sensory guidance of predation by vibrissal information we investigated prey capture by rats after whisker removal and the role of superior colliculus (SC) by comparing Fos expression after hunting with and without whiskers. Rats were allowed to hunt cockroaches, after which their whiskers were removed. Two days later they were allowed to hunt cockroaches again. Without whiskers the rats were less able to retain the cockroaches after capture and less able to pursue them in the event of the cockroach escaping. The predatory behaviour of rats with re-grown whiskers returned to normal. In parallel, Fos expression in SCl induced by predation was significantly reduced in whiskerless animals. We conclude that whiskers contribute to the efficiency of rat prey capture and that the loss of vibrissal input to SCl, as reflected by reduced Fos expression, could play a critical role in predatory deficits of whiskerless rats.

The role of the superior colliculus in predatory hunting.

Combining the results of behavioral, neuronal immediate early gene activation, lesion and neuroanatomical experiments, we have presently investigated the role of the superior colliculus (SC) in predatory hunting. First, we have shown that insect hunting is associated with a characteristic large increase in Fos expression in the lateral part of the intermediate gray layer of the SC (SCig). Next, we have shown that animals with bilateral NMDA lesions of the lateral parts of the SC presented a significant delay in starting to chase the prey and longer periods engaged in other activities than predatory hunting. They also showed a clear deficit to orient themselves toward the moving prey and lost the stereotyped sequence of actions seen for capturing, holding and killing the prey. Our Phaseolus vulgaris-leucoagglutinin analysis revealed that the lateral SCig, besides providing the well-documented descending crossed pathway to premotor sites in brainstem and spinal cord, projects to a number of midbrain and diencephalic sites likely to influence key functions in the context of the predatory behavior, such as general levels of arousal, motivational level to hunt or forage, behavioral planning, appropriate selection of the basal ganglia motor plan to hunt, and motor output of the primary motor cortex. In contrast to the lateral SC lesions, medial SC lesions produced a small deficit in predatory hunting, and compared to what we have seen for the lateral SCig, the medial SCig has a very limited set of projections to thalamic sites related to the control of motor planning or motor output, and provides conspicuous inputs to brainstem sites involved in organizing a wide range of anti-predatory defensive responses. Overall, the present results served to clarify how the different functional domains in the SC may mediate the decision to pursue and hunt a prey or escape from a predator.

Functional mapping of the prosencephalic systems involved in organizing predatory behavior in rats.

The study of the neural basis of predatory behavior has been largely neglected over the recent years. Using an ethologically based approach, we presently delineate the prosencephalic systems mobilized during predation by examining Fos immunoreactivity in rats performing insect hunting. These results were further compared with those obtained from animals killed after the early nocturnal surge of food ingestion. First, predatory behavior was associated with a distinct Fos up-regulation in the ventrolateral caudoputamen at intermediate rostro-caudal levels, suggesting a possible candidate to organize the stereotyped sequence of actions seen during insect hunting. Insect predation also presented conspicuous mobilization of a neural network formed by a distinct amygdalar circuit (i.e. the postpiriform-transition area, the anterior part of cortical nucleus, anterior part of basomedial nucleus, posterior part of basolateral nucleus, and medial part of central nucleus) and affiliated sites in the bed nuclei of the stria terminalis (i.e. the rhomboid nucleus) and in the hypothalamus (i.e. the parasubthalamic nucleus). Accordingly, this network is likely to encode prey-related motivational values, such as prey's odor and taste, and to influence autonomic and motor control accompanying predatory eating. Notably, regular food intake was also associated with a relatively weak Fos up-regulation in this network. However, during regular surge of food intake, we observed a much larger mobilization in hypothalamic sites related to the homeostatic control of eating, namely, the arcuate nucleus and autonomic parts of the paraventricular nucleus. Overall, the present findings suggest potential neural systems involved in integrating prey-related motivational values and in organizing the stereotyped sequences of action seen during predation. Moreover, the comparison with regular food intake contrasts putative neural mechanisms controlling predatory related eating vs. regular food intake.

Predatory hunting and exposure to a live predator induce opposite patterns of Fos immunoreactivity in the PAG.

Considering the periaqueductal gray's (PAG) general roles in mediating motivational responses, in the present study, we compared the Fos expression pattern in the PAG induced by innate behaviors underlain by opposite motivational drivers, in rats, namely, insect predation and defensive behavior evoked by the confrontation with a live predator (a cat). Exposure to the predator was associated with a striking Fos expression in the PAG, where, at rostral levels, an intense Fos expression was found largely distributed in the dorsomedial and dorsolateral regions, whereas, at caudal levels, Fos-labeled cells tended to be mostly found in the lateral and ventrolateral columns, as well as in the dorsal raphe nucleus. Quite the opposite, insect predation was associated with increased Fos expression predominantly in the rostral two thirds of the lateral PAG, where the majority of the Fos-immunoreactive cells were found at the oculomotor nucleus levels. Remarkably, both exposure to the cat and insect predation upregulated Fos expression in the supraoculomotor region and the laterodorsal tegmental nucleus. Overall, the present results clearly suggest that the PAG activation pattern appears to reflect, at least partly, the animal's motivational status. It is well established that the PAG is critical for the expression of defensive responses, and, considering the present findings, it will be important to investigate how the PAG contributes to the expression of the predatory behavior, as well.

Tracing from the dorsal premammillary nucleus prosencephalic systems involved in the organization of innate fear responses.

The dorsal premammillary nucleus (PMd) is thought to play a critical role in the expression of fear responses to environmental threats. We have previously reported that, during an encounter with a predator, the PMd presents an impressive increase in Fos levels and cell body-specific chemical lesions therein virtually eliminated the expression of escape and freezing responses. Therefore, the PMd may be viewed as a strategic starting point to delineate prosencephalic circuits seemingly critical for the organization of innate fear responses. In the present review, we provide a comprehensive examination of the neural circuits putatively involved in influencing this hypothalamic site, and supplement this analysis with recent observations from our laboratory on the expression of Fos protein in the central nervous system of rats exposed to a live predator.

Afferent connections of the dorsal premammillary nucleus.

The dorsal premammillary nucleus (PMd) is thought to play a critical role for the expression of fear responses to environmental threats. We have reported previously that during an encounter with a predator the PMd presents an impressive increase in Fos levels and cell body-specific chemical lesions therein virtually eliminate the expression of escape and freezing responses. In the present study, we carried out a systematic analysis of PMd afferent connections combining anterograde and retrograde tracing methods in the rat. We show that the nucleus receives inputs from several widely distributed areas in the forebrain and, to a much lesser extent, from the brainstem as well. From this information, it seems that the major telencephalic source of input to the PMd is the interfascicular nucleus of the bed nuclei of the stria terminalis. In addition, substantial telencephalic inputs to the nucleus seem to arise from the infralimbic and prelimbic areas, and the lateral septal nucleus. In the diencephalon, massive inputs to the PMd arise from the anterior hypothalamic nucleus, specific parts of the perifornical region, the retinoceptive region of the lateral hypothalamic area, and the anterior and dorsomedial parts of the ventromedial hypothalamic nucleus. In contrast, the ventral tegmental nucleus seems to be the only brainstem site that provides substantial inputs to the PMd. Overall, the present analysis helps to delineate prosencephalic circuits seemingly critical for the organization of innate fear responses to environmental threats, where the PMd presents a major associative role. Furthermore, by means of massive inputs from the ventral tegmental nucleus, the PMd is in a position to integrate information from a neural system involved in spatial working memory, which may be of particular relevance for an effect of attentional mechanisms on the selection of appropriate escape strategies.