Defense-Like Behaviors Evoked by Pharmacological Disinhibition of the Superior Colliculus in the Primate
Stimulation of the intermediate and deep layers of superior colliculus (DLSC) in rodents evokes both orienting/pursuit (approach) and avoidance/flight (defense) responses (Dean et al., 1989). These two classes of response are subserved by distinct output projections associated with lateral (approach) and medial (defense) DLSC (Comoli et al., 2012). In non-human primates, DLSC has been examined only with respect to orienting/approach behaviors, especially eye movements, and defense-like behaviors have not been reported. Here we examined the profile of behavioral responses evoked by activation of DLSC by unilateral intracerebral infusions of the GABA(A) receptor antagonist, bicuculline methiodide (BIC), in nine freely moving macaques. Across animals, the most consistently evoked behavior was cowering (all animals), followed by increased vocalization and escape-like behaviors (seven animals), and attack of objects (three animals). The effects of BIC were dose-dependent within the range 2.5-14 nmol (threshold dose of 4.6 nmol). The behaviors and their latencies to onset did not vary across different infusion sites within DLSC. Cowering and escape-like behaviors resembled the defense-like responses reported after DLSC stimulation in rats, but in the macaques these responses were evoked from both medial and lateral sites within DLSC. Our findings are unexpected in the context of an earlier theoretical perspective (Dean et al., 1989) that emphasized a preferential role of the primate DLSC for approach rather than defensive responses. Our data provide the first evidence for induction of defense-like behaviors by activation of DLSC in monkeys, suggesting that the role of DLSC in responding to threats is conserved across species.
Available from: PubMed Central
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ABSTRACT: Evolutionary conservation of the hypothalamus attests to its critical role in the control of fundamental behaviors. However, our knowledge of hypothalamic connections is incomplete, particularly for the lateral hypothalamic area (LHA). Here we present the results of neuronal pathway-tracing experiments to investigate connections of the LHA juxtaventromedial region, which is parceled into dorsal (LHAjvd) and ventral (LHAjvv) zones. Phaseolus vulgaris leucoagglutinin (PHAL, for outputs) and cholera toxin B subunit (CTB, for inputs) coinjections were targeted stereotaxically to the LHAjvd/v.
LHAjvd/v connections overlapped highly but not uniformly. Major joint outputs included: Bed nuc. stria terminalis (BST), interfascicular nuc. (BSTif) and BST anteromedial area, rostral lateral septal (LSr)- and ventromedial hypothalamic (VMH) nuc., and periaqueductal gray. Prominent joint LHAjvd/v input sources included: BSTif, BST principal nuc., LSr, VMH, anterior hypothalamic-, ventral premammillary-, and medial amygdalar nuc., and hippocampal formation (HPF) field CA1. However, LHAjvd HPF retrograde labeling was markedly more abundant than from the LHAjvv; in the LSr this was reversed. Furthermore, robust LHAjvv (but not LHAjvd) targets included posterior- and basomedial amygdalar nuc., whereas the midbrain reticular nuc. received a dense input from the LHAjvd alone. Our analyses indicate the existence of about 500 LHAjvd and LHAjvv connections with about 200 distinct regions of the cerebral cortex, cerebral nuclei, and cerebrospinal trunk. Several highly LHAjvd/v-connected regions have a prominent role in reproductive behavior. These findings contrast with those from our previous pathway-tracing studies of other LHA medial and perifornical tier regions, with different connectional behavioral relations. The emerging picture is of a highly differentiated LHA with extensive and far-reaching connections that point to a role as a central coordinator of behavioral control.
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ABSTRACT: Many animals avoid dark, approaching objects seen against a lighter background but show no or weaker reactions to stimuli with inverted contrast. We investigated whether human observers would respond differently to such stimuli in terms of estimated time-to-arrival. We varied luminances of an approaching, light or dark disk and a plain, grey background, and for several conditions, continuously adjusted calibrations so as to keep contrast and/or overall lightness constant. Since no effects were found, we conclude that humans are able to discard luminance and contrast for the task at hand. Generally, however, performance was affected by different, consecutive regimes of feedback: Initially, without feedback, observers responded inconsistently and much too late; they improved after correct feedback, and in a third block of trials with pseudo-random feedback, they responded increasingly early without reverting to the initial level of uncertainty. We discuss our findings with regard to implications for neural mechanisms, put them in the context of evolutionary considerations, and propose continuative animal behavioral studies.
Available from: Roland Philipp
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ABSTRACT: Neuronal activity in the deep layers of the macaque (Macaca mulatta) superior colliculus (SC) and the underlying reticular formation is correlated with the initiation and execution of arm movements (Werner, 1993). Although the correlation of this activity with EMGs of proximal arm muscles is as strong as in motor cortex (Werner et al., 1997a; Stuphorn et al., 1999), little is known about the influence of electrical microstimulation in the SC on the initiation and trajectories of arm movements. Our experiments on three macaque monkeys clearly show that arm movements can be elicited by electrical microstimulation in the deep layers of the lateral SC and underlying reticular formation. The most extensively trained monkey, M1, extended his arm toward the screen in front of him more or less stereotypically upon electrical SC stimulation. In two other monkeys, M2 and M3, a larger repertoire of arm movements were elicited, categorized into three movement types, and compared before (M3) and after (M2 and M3) training: twitch (56% vs 62%), lift (6% vs 5%), and extend (37% vs 32%), respectively. Therefore, arm movements induced by electrical stimulation in the monkey SC represent a further component of the functional repertoire of the SC using its impact on motoneurons in the spinal cord, probably via premotor neurons in the brainstem, as well as on structures involved in executing more complex movements such as target-directed reaching. Therefore, the macaque SC could be involved directly in the initiation, execution, and amendment of arm and hand movements.
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