Evidence for a hypothalamothalamocortical circuit mediating pheromonal influences on eye and head movements.

Abstract

A method for simultaneous iontophoretic injections of the anterograde tracer Phaseolus vulgaris leukoagglutinin and the retrograde tracer fluorogold was used to characterize in the rat a hypothalamothalamocortical pathway ending in a region thought to regulate attentional mechanisms by way of eye and head movements. The relevant medial hypothalamic nuclei receive pheromonal information from the amygdala and project to specific parts of the thalamic nucleus reuniens and anteromedial nucleus, which then project to a specific lateral part of the retrosplenial area (or medial visual cortex). This cortical area receives a convergent input from the lateral posterior thalamic nucleus and projects to the superior colliculus. Bidirectional connections with the hippocampal formation suggest that activity in this circuit is modified by previous experience. Striking parallels with basal ganglia circuitry are noted.The organization of circuits that mediate orienting responses to somatosensory, visual, and auditory stimuli is known at least in outline, with important components including the thalamus, motor cortical areas, and superior colliculus (1, 2). In contrast, almost nothing is understood about how pheromonal and other olfactory stimuli, which in rodents are particularly important for reproductive, aggressive, and ingestive behaviors, influence eye and head movements. Pheromonal information is relayed by sexually dimorphic pathways involving the vomeronasal organ, accessory olfactory bulb, and corticomedial amygdala to the medial zone of the hypothalamus, but there is little evidence for projections from this circuitry to thalamic, cortical, and midbrain regions concerned directly with regulating eye and head movements and, thus, visuomotor and directed attentional mechanisms (3, 4).We have recently identified dense projections from three adjacent, highly interconnected medial hypothalamic nuclei (anterior, ventromedial, and dorsal premammillary) to two adjacent nuclei of the rostral thalamus, the rostral nucleus reuniens (REr) and ventral anteromedial nucleus (AMv) (5-7). In the work presented here, a method for simultaneous injection into the same site of the anterograde axonal tracer Phaseolus vulgaris leukoagglutinin (PHAL) and the retrograde axonal tracer fluorogold (FG) was used to characterize the hypothalamic and cortical interconnections of the REr. At the cortical level, the method was used to define the connections of a very restricted area that receives a convergent input from the REr and lateral posterior thalamic nucleus (LP) and that projects back to the LP and superior colliculus. On cytoarchitectonic grounds, this cortical area has previously been regarded as either the lateralmost part of the retrosplenial area (RSP) or the medialmost part of the visual cortex in the rat or mouse (for example, see refs. 8 and 9).The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 sole...

Projections of the medial orbital and ventral orbital cortex in the rat

“…RSCagl is reportedly an integral part of a distributed circuitry subserving defensive behaviors (Carvalho-Netto et al, 2010). Swanson and colleagues (Risold and Swanson, 1995;Risold et al, 1997) described reciprocal connections between MO/VO and RSCagl, but less pronounced MO/VO projections to RSCagl than shown here. More recently, however, Shibata and Naito (2008) demonstrated substantial ORB projections to RSCagl (or area 29d) and further showed that MO primarily targets the rostral two-thirds of area 29d and VO the caudal one-third of area 29d.…”

Afferent projections to nucleus reuniens of the thalamus

“…proposed that the hypothalamus is organized into three longitudinally aligned functional zones (periventricular, medial, and lateral) and that the medial hypothalamus can be divided into caudal and rostral regions-a caudal zone associated with Papez's circuit and a rostral one primarily involved in reproductive, defensive, and homeostatic behaviors. Risold and Swanson (1995) further suggested that RE may serve a unique role in certain behaviors associated with the medial hypothalamus, namely, mediating olfactory (pheromonal) influences on eye and head movements during orientation. Specifically, they postulated that pheromonal information is transmitted from olfactory structures (and from basomedial amygdala) to nuclei of the medial hypothalamus (mainly to AHN, VMH, PH, and PMd) and from there to RE and to the anteromedial nucleus (AM) of thalamus.…”

“…Risold and Swanson (1995) described a circuit mediating olfactory influences on eye and head movements that, in part, involves reciprocal RE connections with lateral aspects of the agranular retrosplenial cortex (RSCagl). They demonstrated moderate RSCagl projections to RE, predominantly targeting the rostral pole of RE.…”

New Perspectives on β-Adrenergic Mediation of Innate and Learned Fear Responses to Predator Odor

“…Whereas the PAG appears to influence antipredatory defensive responses (Cezario et al, 2008), the ventral part of the anteromedial thalamic nucleus projects to the lateral retrosplenial area and is thought to be involved in modulating the eye and head movements associated with attentional processes (Risold and Swanson, 1995). In fact, we have shown recently that the PMd influences the activation of its major projecting targets in response to predatory threats (i.e., the PAG and the ventral part of the anteromedial thalamic nucleus) but does not seem to affect the amygdalar sites involved in predator's cue detection (Cezario et al, 2008).…”