Afferent connections of the amygdalopiriform transition area in the rat

Abstract

The amygdalopiriform transition area (APir) is often considered part of the lateral entorhinal cortex (Entl). However, in contrast to Entl, APir densely innervates the central extended amygdala (EAc) and does not project to the dentate gyrus. In order to gain a more comprehensive understanding of these territories, the afferent connections of APir were examined in the rat with retrograde (cholera toxin B subunit or FluoroGold) and anterograde tracers (Phaseolus vulgaris leucoagglutinin) and compared to those of the neighboring Entl. The results suggest that APir and Entl are interconnected and receive topographically organized hippocampal projections. Both are targeted by the olfactory bulb, the piriform, posterior agranular insular and perirhinal cortices, the ventral tegmental area, dorsal raphe nucleus, and locus coeruleus. Most importantly, the data reveal that APir and Entl also have specific inputs and should be viewed as separate anatomical entities. The APir receives robust projections from structures affiliated with the EAc, including the anterior basomedial and posterior basolateral amygdaloid nuclei, the gustatory thalamic region, parasubthalamic nucleus, and parabrachial area. The Entl is a major recipient for amygdaloid projections from the medial part of the lateral nucleus and the caudomedial part of the basolateral nucleus. Moreover, the medial septum, subicular complex, nucleus reuniens, supramammillary region, and nucleus incertus, which are associated with the hippocampal system, preferentially innervate the Entl. These data underscore that APir processes olfactory and gustatory information and is tightly linked to EAc operations, suggesting that it may play a role in reward mechanisms, particularly in hedonic aspects of feeding.

Hippocampal Formation

“…Minor inputs arise from other the other midline thalamic nuclei, like the paraventricular, the paratenial and the intermediodorsal nucleus. The paraventricular nucleus sparsely innervates LEC and MEC, projections from the paratenial nucleus are moderate to dense in LEC, while those from the intermediodorsal nucleus to LEC are moderate (Van der Werf et al, 2002;Santiago and Shammah-Lagnado, 2005). Most nuclei of the intralaminar thalamic nuclei, the paracentral ( Van der Werf et al, 2002), the central medial (Santiago and Shammah-Lagnado, 2005;Vertes et al, 2012) and the parafasicular nucleus ( Van der Werf et al, 2002;Santiago and Shammah-Lagnado, 2005) sparsely innervate EC.…”

“…HYPOTHALAMUS The EC receives diffuse inputs from various structures in the hypothalamus (Segal, 1977;Swanson, 1982;Santiago and Shammah-Lagnado, 2005;Kerr et al, 2007), mainly targeting lateral and caudodorsal parts of MEC (Kerr et al, 2007). These include afferents from: (1) The supramammillary nucleus that terminate rather diffusely with some preference for layers III-VI (Haglund et al, 1984;Santiago and ShammahLagnado, 2005); (2) The tuberomammillary nucleus distributing diffusely in LEC and MEC (Saper, 1985;Santiago and Shammah-Lagnado, 2005); and (3) the lateral hypothalamic area reaching preferentially the deep layers of EC Saper, 1985;Santiago and Shammah-Lagnado, 2005).…”

“…Although initially no inputs from the anterior thalamic complex have been reported (Segal, 1977;Beckstead, 1978;Wyss et al, 1979b), later studies showed that layer V of the EC receives weak inputs from the anteromedial (Shibata, 1993;Shibata and Kato, 1993;Van Groen et al, 1999), anterodorsal (Shibata, 1993;Van Groen and Wyss, 1995), and anteroventral nuclei ( Shibata, 1993;Van Groen and Wyss, 1995). HYPOTHALAMUS The EC receives diffuse inputs from various structures in the hypothalamus (Segal, 1977;Swanson, 1982;Santiago and Shammah-Lagnado, 2005;Kerr et al, 2007), mainly targeting lateral and caudodorsal parts of MEC (Kerr et al, 2007). These include afferents from: (1) The supramammillary nucleus that terminate rather diffusely with some preference for layers III-VI (Haglund et al, 1984;Santiago and ShammahLagnado, 2005); (2) The tuberomammillary nucleus distributing diffusely in LEC and MEC (Saper, 1985;Santiago and Shammah-Lagnado, 2005); and (3) the lateral hypothalamic area reaching preferentially the deep layers of EC Saper, 1985;Santiago and Shammah-Lagnado, 2005).…”

“…Termination occurs preferentially in the deep layers of LEC and MEC (Eid et al, 1996;Behan and Haberly, 1999) and scarcer labeling was found in layer I and III (Krettek and Price, 1977;Eid et al, 1996;Behan and Haberly, 1999). THALAMUS Major thalamic input to EC originates from two midline thalamic nuclei: the nucleus reuniens and the rhomboid nucleus (Beckstead, 1978;Herkenham, 1978;Wouterlood et al, 1990;Wouterlood, 1991;Santiago and Shammah-Lagnado, 2005;Vertes et al, 2006Vertes et al, , 2012see Thalamus, Chapter 16). The rhomboid nucleus project to layer I and V of mainly LEC ( Van der Werf et al, 2002;Vertes et al, 2006).…”

The rat perirhinal cortex: A review of anatomy, physiology, plasticity, and function

“…Additionally, the majority of projections from the perirhinal cortex to the entorhinal cortex terminate in the lateral entorhinal cortex (Naber et al, 1997;Santiago and Shammah-Lagnado, 2005). Cells from the rostral perirhinal cortex innervate rostral regions of the lateral entorhinal cortex and likewise those from the caudal perirhinal cortex go to caudal areas of the entorhinal cortex (Burwell and Amaral, 1998a).…”