Projection to the inferior colliculus from the basal nucleus of the amygdala

Abstract

This report describes a projection from the amygdala, a forebrain center mediating emotional expression, to the inferior colliculus (IC), the midbrain integration center of the ascending auditory system. In the IC of mustached bats (Pteronotus parnellii) and pallid bats (Antrozous pallidus), we placed deposits of retrograde tracers at physiologically defined sites and then searched for retrogradely labeled somata in the forebrain. Labeling was most sensitive in experiments using cholera toxin B-subunit as tracer. We consistently observed retrograde labeling in a single amygdalar subdivision, the magnocellular subdivision of the basal nucleus (Bmg). The Bmg is distinctive across mammals, containing the largest cells in the amygdala and the most intense acetylcholinesterase staining. Labeled amygdalar cells occurred ipsilateral and contralateral to IC deposits, but ipsilateral labeling was greater, averaging 72%. Amygdalar labeling was observed after tracer deposits throughout the IC, including its central nucleus (ICC). In comparison, labeling in the auditory cortex (layer V) was heavily ipsilateral (averaging 92%). Cortical labeling depended on the location of IC deposits: dorsomedial deposits resulted in the most labeled cells, whereas ventrolateral deposits labeled few or no cortical cells. Cortical labeling occurred after several deposits in the ICC. Across experiments, the average number of labeled cells in the amygdala was similar to that in the auditory cortex, indicating that the amygdalocollicular projection is significant. The results demonstrate a direct, widespread projection from the basal amygdala to the IC. They also suggest the presence of a rapid thalamoamygdalocollicular feedback circuit that may impose emotional content onto processing of sensory stimuli at a relatively low level of an ascending sensory pathway.

Fig. 1.

Views of the amygdala and other forebrain structures in mustached and pallid bats. A, Nissl-stained coronal section in the mustached bat shows large lateral nucleus (L) and darkly stained magnocellular division of the basal nucleus (Bmg). B, Cholinesterase-stained section in mustached bat shows staining of Bmg and caudate–putamen. Section is from a different animal than the section in A. C, Nissl-stained coronal section in the pallid bat. D, Cholinesterase-stained section in the pallid bat shows staining of Bmg and caudate–putamen. Sections in C and D are from the same animal. Protocol for photomicrographs is as follows (plan apochromat):A, C, NA 0.08; B,D, NA 0.16. The following anatomic abbreviations are used throughout figure legends: AB, accessory basal nucleus of the amygdala; ALD, anterolateral division of the central nucleus of the inferior colliculus; Bmg, magnocellular subdivision of the basal nucleus of the amygdala;Bpc, parvicellular subdivision of the basal nucleus of the amygdala; CE, central nucleus of the amygdala;COp, posterior cortical nucleus of the amygdala;CPu, caudate–putamen; DC, dorsal cortex of the inferior colliculus; DPD, dorsoposterior division of the central nucleus of the inferior colliculus; ec, external capsule; En, endopiriform nucleus;Ex, external nucleus of the inferior colliculus;Hip, hippocampal formation; Hyp, hypothalamus; I, intercalated nuclei of the amygdala; IC, inferior colliculus; ICC, central nucleus of the inferior colliculus; int, internal capsule; L, lateral nucleus of the amygdala;ll, lateral lemniscus; LV, lateral ventricle; M, medial nucleus of the amygdala;MD, medial division of the central nucleus of the inferior colliculus; MGB, medial geniculate body;opt, optic tract; PAC, periamygdaloid cortex; PAG, periaqueductal gray; Pir, piriform cortex; rf, rhinal fissure; Tem, temporal cortex; wm, white matter underlying cerebral cortex.

Fig. 2.

Location of tracer deposits and tonotopic organization in the IC of mustached bats (A,B) and pallid bats (C, D).A, Schematic view of the tonotopic organization in mustached bat's IC, with location of CTb tracer deposits indicated. Frequencies in lower part of audible range (10–59 kHz) are represented systematically in the anterolateral division (ALD) of ICC. The dorsoposterior division (DPD) disproportionately represents frequencies in the 59–63 kHz range, whereas frequencies >63 kHz are represented in the medial division (MD). B, Deposit of CTb in a mustached bat's ICC at site tuned to 86.1 kHz (case 5).C, Schematic view of the tonotopic organization of the pallid bat's IC, with the location of CTb tracer deposits indicated.D, Deposit of CTb in a pallid bat's ICC at site tuned to 41.9 kHz (case 20). In A andC, gray lines and textindicate isofrequency lines in the IC. Protocol for all photomicrographs is as follows (plan apochromat): NA 0.16.

Fig. 3.

Retrograde labeling in Bmg after tracer deposits in the IC. A, C, Lower-power (A) and higher-power (C) views of retrograde labeling in the ipsilateral Bmg of the mustached bat after the CTb deposit illustrated in Figure2B. B, D, Lower-power (B) and higher-power (D) views of retrograde labeling in the ipsilateral Bmg of the pallid bat after the CTb deposit illustrated in Figure 2D. Retrograde neuronal labeling is restricted to the Bmg. Examples of artifactual label are evident in C (far left) and D (top). Protocol was as follows (plan apochromat): A, B, NA 0.08; C, D, NA 0.40.

Fig. 4.

Distribution of retrograde label in the amygdala after tracer deposits in the IC. A, Labeling in a mustached bat after tracer deposit shown in Figure2B. B, Labeling in a pallid bat after tracer deposit shown in Figure 2D. Sections are arranged from caudal (top) to rostral (bottom), and the labeling on the side ipsilateral to the deposit is presented on the left. In both experiments, labeling was bilateral with an ipsilateral predominance. Outline of the Bmg is in bold.

Fig. 5.

Caudal-to-rostral pattern of retrograde labeling in Bmg. Retrograde labeling is expressed as the percentage of total labeling in increments of the caudal-to-rostral extent of the entire basal nucleus. A, Labeling in the mustached bat on the ipsilateral (IPSI) and contralateral (CONTRA) sides. B, Labeling in the pallid bat. Black arrowheads indicate the caudal and rostral borders of the Bmg as discussed in Results (lower tip indicates average border across animals; top, lateral tips indicate range of borders).

Fig. 6.

Retrograde labeling in ipsilateral auditory cortex after CTb tracer deposits in the IC. Roman numeralsindicate cortical layers. A, Labeling in a mustached bat (Fig. 2A,B, case 5). Retrograde transport to the amygdala after the ICC deposit is shown in Figures 3A and 4A.B, Labeling in a mustached bat (Fig.2A, case 2). C, Labeling in a pallid bat (Fig. 2C,D,case 20). Retrograde transport to the amygdala after the ICC deposit is shown in Figures 3B and 4B. D, Labeling in a pallid bat (Fig. 2C, case 13) after four CTb deposits in regions tuned near 15 kHz. Protocol for all photomicrographs was as follows (plan apochromat): NA 0.16.

Fig. 7.

Comparison of retrograde labeling in brainstem, auditory cortex, and amygdala after CTb deposits in the IC of mustached bats and pallid bats. The relative distribution of label in the two species is nearly identical, despite wide variation among individual cases. Columns indicate average percentage of labeling in the three brain regions; vertical lines indicate the range of values.

Fig. 8.

Summary of the neural connections demonstrated in this article. Both the auditory cortex and basal nucleus of the amygdala project to the IC bilaterally. The strongest projection, in terms of the number of projection neurons, is the ipsilateral auditory cortex, followed in descending order by the ipsilateral Bmg, contralateral Bmg, and contralateral auditory cortex.

Fig. 9.

Paths by which auditory information is processed in the amygdala and projected back to the IC. Solid lines indicate feedforward projection of auditory information.Dotted lines indicate feedback connections that can include results of amygdalar processing. Sources are as follows: projections from auditory cortex and amygdala to IC (present study); projections from MGB to amygdala in rats (LeDoux et al., 1985); projections from auditory cortex to amygdala in the mustached bat (Fitzpatrick et al., 1998) and in monkeys (Aggleton et al., 1980;Stefanacci and Amaral, 2000); projections from the amygdala, including Bmg, to auditory cortex in other species (Amaral and Price, 1984;McDonald and Jackson, 1987); many additional connections exist between amygdaloid nuclei and auditory cortex.