Neural substrates for tongue‐flicking behavior in snakes

Abstract

Snakes deliver odorants to the vomeronasal organ by means of tongue-flicks. The rate and pattern of tongue-flick behavior are altered depending on the chemical context. Accordingly, olfactory and vomeronasal information should reach motor centers that control the tongue musculature, namely, the hypoglossal nucleus (XIIN); however, virtually nothing is known about the circuits involved. In the present work, dextran amines were injected into the tongue of garter snakes (Thamnophis sirtalis) to identify the motoneurons of the XIIN. Tracers were then delivered into the XIIN to identify possible afferents of chemical information. Large injections into the XIIN yielded retrograde labeling in two chemosensory areas: the medial amygdala (MA) and the lateral posterior hypothalamic nucleus (LHN). Smaller injections only yielded labeled neurons in the LHN. In fact, the MA, which receives afferents from the accessory olfactory bulb, the rostroventral lateral cortex, and the nucleus sphericus, projects to the LHN. Injections into the MA did not show terminal labeling in the XIIN but in an area lateral to it. However, injections into the LHN gave rise not only to labeled fibers in the XIIN but also to retrograde labeling in the MA, thus confirming the chemosensory input to LHN. Injecting different fluorescent tracers into the tongue and into the LHN corroborated the projection from the LHN to the XIIN. The present report investigates further connections of the olfactory and vomeronasal systems and describes the afferent connections to XIIN in a nonmammalian vertebrate. The circuit for tongue-flicking behavior described herein should be evaluated using functional studies.

Efferent connections of the “olfactostriatum”: A specialized vomeronasal structure within the basal ganglia of snakes

“…Accordingly, vomeronasal, and probably also olfactory information, most likely influence motor centers that control tongue musculature, namely, the XIIN. In a previous paper, a possible circuit for vomeronasal influence on tongueflicking behavior was described (Martínez-Marcos et al, 2001). Such a circuit included the projection from the MA, which receives vomeronasal information from the AOB (Lanuza and Halpern, 1998) and olfactory information from the LCRV (Martínez-Marcos et al, 1999), to the LHN, which in turn projects to the XIIN (Martínez-Marcos et al, 2001).…”

“…9). Since the LHN as a whole projects to the XIIN (Martínez-Marcos et al, 2001), the possibility arises that both the MA/BNST and the OS provide chemosensory information to the LHN, which in turn could influence the XIIN activity. In this scenario, the MA/BNST would relay vomeronasal and olfactory information to the LHN, whereas the OS would participate in reinforcing circuits (Halpern, 1988) and influence motor control of tongueflicking behavior.…”

“…In a previous paper, a possible circuit for vomeronasal influence on tongueflicking behavior was described (Martínez-Marcos et al, 2001). Such a circuit included the projection from the MA, which receives vomeronasal information from the AOB (Lanuza and Halpern, 1998) and olfactory information from the LCRV (Martínez-Marcos et al, 1999), to the LHN, which in turn projects to the XIIN (Martínez-Marcos et al, 2001). Interestingly, in the present study we have found a projection from the OS to the LHN, the terminal field of which is adjacent within this nucleus to the terminal field of the projection originating from the MA/ BNST (Fig.…”

“…For instance, a pathway from the MA to the lateral posterior hypothalamic nucleus (LHN) and from there to the hypoglossal nucleus (XIIN) was described as a possible pathway for vomeronasal influence on tongue-flick behavior (Martínez-Marcos et al, 2001). Herein, we have investigated the possibility of a comparable pathway through the OS.…”

Neurobiology of Seasonal Life-history Transitions

“…Because only NPY cells, and not AVT cells, occur in the medial cortex and NS, I distinguished the boundaries of these regions using the same brain atlas used for counting NPY cells Krohmer et al, 2010;Martínez-Marcos et al, 2001), and then outlined the region of interest and measured its area using the calibrated measure feature of ImageJ software (NIH); I repeated this procedure for every tissue section containing the region of interest.…”