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Anatomic and functional study of the closed-loop connection between basal ganglia and superior colliculus during predatory behavior in rats

Abstract

In a recent study, examining the expression of Fos protein, we studied the key neural systems mobilized during predatory behavior of rats hunting roaches. Of particular interest, we have found that predatory hunting induces a distinct activation of the lateral region of the superior colliculus (SCI), which does not appear to be particularly mobilized in other behavioral situations, such as after nocturnal peak of food ingestion. In order to understand the potential roles of this collicular region in the context of predatory hunting, we first analyzed the hunting performance of the animals before and after iontophoretic NMDA lesions bilaterally placed into SCI. Notably, collicular lesions did not interfere with the motivation to pursue the roaches, however, they did induce severe deficits related to motor praxia, i.e, lesioned animals handled the preys very awkwardly and were unable to capture and hold them efficiently. In addition, lesioned animals could not properly orient themselves toward fast moving roaches. We next examined the conceptions of SCI. Efferent projections of the SCI which were analyzed by using the PHA-L method, suggest that SCI appear to influence the motor output via two main pathways: a descending putative involved in coordinating eyes, orofacial and forelimb orienting movements toward the moving preys; and ascending pathways, which is in a position to modulate motor responses by influencing thalamic regions also targeted by the basal ganglia and cerebellum. Experiments with the retrograde tracer Fluoro-Gold showed that the SCI, likewise structures related to motor control, receives information related to somatosensory sensibility from the whiskers and orofacial region. Finally, our anterograde findings also revealed direct projection from SCI to the compact part of substantial nigra (SNc), and we were able to show that SCI supply direct innervations to dopaminergic cells in the midbrain, and also electrophysiological relations. Therefore, he SCI may as well convey multimodal sensory information to dopaminergic cells, exerting a critical role in controlling intentional mechanisms and motor strategies shifts. MCHAFFIE et al., proposed that phylogenetic old cIosed-loop connections exist between the basal ganglia and brain stem sensory related structures like superior colliculus(SC), however the full extent to which they actually represent functionally segregated parallel closed-loop remains to be determined. So, in attempt to better understand the role of SC, we intend to verify functional aspects of connections between SC and basal ganglia during predation. To this investigation animals will be prepared with chronic guide-cannulae providing access to thalamic nuclei, which provide the main excitatory inputs to striatum. Stimulation of SCI by the presence of preys and innativation of thalamic regions target by SCI y injecting mucimol would have a corresponding greater effect on predation. In order to define thalamic sites to receive mucimol we will inject PHA-I in SCI and find out whether anterograde fibers merge cells expressing Fos during predation in a topographic way. Of our interest, we will check for possible neurotransmitters involved in the SCI projections to thalamus related predation, like galanin, NPY, substantia P, neurotensin, somatostatin, CCK, dynorphin, and enkephalin. For this series of experiments we will inject CTb in thalamic sites previously defined and do immunofluorescent triple dettection in SCI for CTb, the phenotypes mentioned and Fos expression in rats after hunting roaches and describe labels pattern. And, finally, we intend to check whether same cells in SCI project to thalamus and compact part of substantia nigra. For this experiment we will have animals ipsilaterally double injected of CTb in thalamic nuclei and FG in compact part of substantia nigra and will triple detect SCI for CTb, FG and Fos after hunting roaches, using fluorescent methods and describe labels pattern. (AU)

Articles published in Agência FAPESP Newsletter about the research grant:
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Scientific publications
(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)
COMOLI, ELIANE; FAVARO, PLINIO DAS NEVES; VAUTRELLE, NICOLAS; LERICHE, MARIANA; OVERTON, PAUL G.; REDGRAVE, PETER. Segregated anatomical input to sub-regions of the rodent superior colliculus associated with approach and defense. FRONTIERS IN NEUROANATOMY, v. 6, . (06/03655-4)