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Afferent and efferent connections
- The Amygdaloid Complex: Anatomy and Physiology

Data on afferent and efferent connections to the amygdaloidcomplex come from studies in which anterograde or retrogradetracers have been injected into various amygdaloid, cortical,and subcortical regions. These studies reveal that each amygdaloidnucleus receives inputs from multiple yet distinct brain regions(159, 208, 213). Efferent projections from the amygdala arealso widespread and include both cortical and subcortical regions(208). There is a vast and complex literature on connectionsinvolving the amygdaloid complex, and there have recently beentwo detailed reviews (159, 208). Here we briefly summarizethe main afferent and efferent connections to the amygdala.Studies carried out in rats, cats, and monkeys show that inmost cases there are extensive similarities in the organizationof inputs and outputs in the three species. We have chosento concentrate on the connections in the rat, since most ofthe physiology has been performed in this species.

Based largely on the information content of the afferents, inputsto the amygdala can be separated into those arising in corticaland thalamic structures and those arising in the hypothalamusor brain stem. Cortical and thalamic inputs supply informationfrom sensory areas and structures related with memory systems.Hypothalamic and brain stem inputs arise from regions involvedin behavior and autonomic systems. The major source of sensoryinformation to the amygdala is the cerebral cortex (159).These projections are glutamatergic, predominantly arisingfrom layer V pyramidal neurons (7, 194). The majority areipsilateral and enter the amygdala via the external capsule(145). Most cortical projections originate in associationareas and transmit processed information by a series of cortico-corticalconnections originating in the primary sensory cortex. Theseinputs can be divided into those that relay modality-specificsensory information, those that are polymodal, and those arisingin the medial temporal lobe memory system. The different inputsand their distributions in the amygdala are summarized in Figure 2.


A. Sensory Inputs

The amygdala receives inputs from all modalities: olfactory,somatosensory, gustatory and visceral, auditory, and visual.

Olfactory projections arise from the main and accessory olfactorybulbs as well as the primary olfactory cortex. The main olfactorybulb projects mainly to the nucleus of the lateral olfactorytract, anterior cortical nucleus, and the periamygdaloid cortex,whereas the accessory olfactory bulb projects to the bed nucleusof the accessory olfactory tract, the medial nucleus, and posteriorcortical amygdala (250). The piriform cortex and anteriorolfactory nucleus have projections to the lateral amygdala,basal, and accessory basal nuclei (131). The dorsal endopiriformnucleus additionally projects to all cortical nuclei of theamygdala as well as the nucleus of the lateral olfactory tract,the periamydaloid cortex, and medial amygdala (12). Thus allregions of the olfactory stream have projections to the amygdaloidcomplex.

For somatosensory inputs, few projections arise directly fromprimary somatosensory areas. Most afferents reach the amygdalavia the dysgranular parietal insular cortex in the parietallobe (256). These projections target the lateral, basal, andcentral nucleus (162, 256, 255). For the lateral amygdala,strong labeling is seen in the dorsolateral subdivision whilein the basal nucleus these inputs are not segregated (256).Somatosensory information also reaches the amygdala by projectionsfrom the pontine parabrachial nucleus and thalamic nuclei,the medial portion of the medial geniculate and the posteriorinternuclear nucleus (PIN), which have been suggested to beinvolved in the transmission of nociceptive information (16,19, 121). Inputs arising in the PIN target all subdivisionsof the LA, but also innervate the accessory basal nucleus andthe medial subdivision of the central nucleus (15, 129).

Gustatory and visceral primary areas in the anterior and posteriorinsular cortices provide strong projections to the dorsal subdivisionof LA, posterior basal nucleus, and central nucleus (255).Gustatory and visceral information also arrive from subcorticalstructures and, as with somatosensory projections, both corticaland subcortical inputs converge in the amygdaloid complex (159).Inputs from the posteromedial ventral thalamic nucleus (thethalamic gustatory nucleus) terminate in the LA, B, and CeL(185, 274), and those from the parabrachial nucleus, whichreceives projections from the nucleus of the solitary tract,target the CeL (15, 193).

Auditory and visual information also reach the amygdala fromassociation areas rather than primary cortex. These pathwaysare thought to be particularly relevant during fear conditioning(see below). For auditory information, area Te1, the primaryauditory cortex in rat, has no direct projections to the amygdala(145, 254). Injections of anterograde tracers in Te3 showfibers in the LA, with the dorsolateral subdivision being themost common target (119, 254). Retrograde tracing studieshave shown that these projections arise from cortical layersII and IV (119). Subcortical acoustic inputs arise from thethalamic medial geniculate nucleus and target the same areasof the LA (118, 119, 274). As with acoustic inputs, visualcortical projections to the amygdala also originate both fromthalamic and high-order visual areas (253). Cortical projectionsfrom these areas (Oc2) follow a cascade to the amygdala inlarge part via Te2 (159, 253). These fibers terminate inthe dorsal subdivision of the LA, the CeL, and some in the magnocellularbasal nucleus.

B. Polymodal Inputs

There are several sources of polymodal sensory information tothe amygdala. These include prefrontal cortex, perirhinal cortex,and hippocampus. The prefrontal cortex is a major source ofcortical projections to the amygdaloid complex. Informationfrom all sensory modalities converges in the prefrontal corticalareas (224), many of which are involved in behavior and rewardcircuitry in rats (231). In all species, a dense and topographicallyorganized projection from the frontal cortex has been described(159). The basal nucleus is the main target of afferents fromthe prefrontal cortex, although projections to the LA as wellas accessory basal, central, and medial nuclei have also beendescribed (165).

Areas related to the long-term declarative memory system includethe perirhinal cortex, the entorhinal cortex, the parahippocampalcortex, and the hippocampus (175). Projections between theamygdala and these structures are reciprocal and strong (159,208). The medial division of the LA receives the heaviestprojection from the perirhinal cortex, but projections to basaland cortical nuclei have also been described (257). The entorhinalcortex in comparison appears to project to most amygdalar nuclei(164). Inputs from hippocampus to the amygdala mainly originatein the subicular region, and although the basal nucleus isthe main target, most other nuclei are also more sparsely innervated(26).

In summary, the amygdala receives sensory information from allmodalities. These inputs target structures in the amygdaloidcomplex at all levels, from the traditionally considered inputside of the complex (basolateral complex and cortical nuclei)to the output side (centromedial nuclei) (208). Thus thereare extensive levels of convergence between different sensorymodalities. In combination with access to information fromthe medial temporal memory systems, the amygdala is in a goodposition to form associations between current sensory inputsand past experience.

In addition to sensory information, the central, lateral, andmedial nuclei receive substantial inputs from the hypothalamuswhile the other amygdalar areas receive very meager projections.For brain stem inputs, the central nucleus is a major targetfor a variety of inputs from the midbrain, pons, and medulla,while the other nuclei receive few or no inputs from these areas(208).

C. Efferent Connections

The amygdaloid nuclei have widespread projections to cortical,hypothalamic, and brain stem regions (Fig. 3). In general,projections from the amygdala to cortical sensory areas arelight and originate in cortical and basolateral areas of theamygdala. The perirhinal area, along with other areas in thefrontal cortex that project to the amygdala, receive reciprocalconnections from the LA, B, AB, M, and periamygdaloid cortex(208). The cortical nuclei that receive olfactory projectionsall send substantial reciprocal projections back to the olfactorycortex.

The basolateral complex (LA, B, AB) has a substantial projectionto the medial temporal lobe memory system with afferents tohippocampus and perirhinal cortex (205, 208). A large projectionis also found to the nucleus accumbens (154). Similar to theLA, the basal nucleus also has substantial projections to hippocampus,but in addition has a major projection to prefrontal cortex,nucleus accumbens, and the thalamus. Efferents from the basolateralcomplex arise from pyramidal-like neurons and are thought tobe glutamatergic (204).

As mentioned above, the amygdala is involved in emotional responses,especially in fear and fear conditioning. These responses arecharacterized by freezing, potentiated startle, release ofstress hormones, and changes in blood pressure and heart ratewhich are elicited by activation of the autonomic and hormonalsystems (42, 115). Activation of the central nucleus inducesthis autonomic response by stimulating groups of neurons inthe brain stem that control the autonomic system, or alternativelyby stimulating hypothalamic nuclei that modulate these centers(97, 120). In agreement with these behavioral responses,the medial subdivision of the central nucleus has substantialprojections to the hypothalamus, bed nucleus of the stria terminalis(49), and several nuclei in the midbrain, pons, and medulla(279). Projections to the brain stem are to three main areas:the periaqueductal gray, which leads to vocalization, startle,analgesia and cardiovascular changes (13, 226); the parabrachialnucleus, which is involved in pain pathways (67, 178); andthe nucleus of the solitary tract (NTS), which is connectedwith the vagal system (275).

The hypothalamus contains a group of nuclei that have a majorinfluence in the coordination of ingestive, reproductive, anddefensive behaviors (267). The medial and capsular subdivisionsof the central nucleus innervate mostly the dorsolateral andcaudolateral regions of the hypothalamus (205). These areasof the hypothalamus project to autonomic cell groups in thebrain stem and spinal cord (268). Efferents from the lateralsubdivision of the central nucleus and from nuclei related withthe olfactory system in the amygdala also project to theseareas. Other hypothalamic nuclei innervated by the amygdalaare the medial nuclei of the behavior control column (205).The ventromedial nucleus, which is involved in reproductivebehavior, is also innervated by nuclei related to the olfactorysystem in the amygdala, particularly the medial nucleus, posteriorbasal nucleus, and posterolateral cortical nucleus. The medialnucleus also sends projections to the hypothalamic neuroendocrinezone, mainly to the anterior paraventricular nucleus (45,205).

In addition to these direct projections to the hypothalamus,the CeA has a strong projection to the BNST, which also innervateshypothalamic nuclei. Furthermore, both CeA and BNST have strongprojections to ascending monoaminergic and cholinergic neurongroups. These include the noradrenergic locus coeruleus, thedopaminergic substantia nigra and ventral tegmental area, theserotonergic raphae, and the cholinergic nucleus basalis (8,43, 213). These systems innervate large regions of the forebrainand temporal lobe memory systems as well as providing inputsto the amygdaloid complex. Rather than the fast, point-to-pointexcitation mediated by most glutamatergic afferents, these ascending systems provide modulatory inputs that affect informationprocessing over large cell assemblies.

Large numbers of neurons in the medial subdivision of the centralnucleus and medial nucleus are GABAergic, and these projectionsfrom the central nucleus have been suggested to be inhibitory(209, 244). Functionally, activation of CeA neurons in therat results in rises in blood pressure and heart rate. A GABAergicprojection from the CeA suggests these fibers are likely toinnervate local inhibitory cells in brain stem nuclei. However,no direct evidence for this is available.

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