Tract tracing studies have revealed that amygdala nuclei have
extensive intranuclear and internuclear connectivity (105
). These studies indicate that sensory information enters
the amygdala through the basolateral nuclei, is processed locally,
and then follows a predominantly lateral to medial progression
to the centromedial nuclei which act as an output station (210
However, little is known about the synaptic physiology of these
circuits in the amygdala and how these networks integrate incoming
information. The connections between the different nuclei in
the amygdala have been described in great detail (208
Here we summarize results (Fig. 4
) obtained in the rat, although
data are also available in cat (105
). We restrict the discussion to connections involving
the basolateral complex and centromedial nuclei since these
nuclei are the best understood functionally.
Within the LA, extensive rostrocaudal as well as interdivisionalconnections have been described (211). The dorsolateral subdivisionprojects to the medial subdivision and to lateral aspects ofthe lateral subdivision. As described above, unimodal sensoryinputs enter the LA laterally while the polymodal afferentsand projections from declarative memory systems are largelyconfined to the medial subdivision (208). The presence of thelateral to medial intranuclear connections within the LA suggestthat the medial subdivision might be a site for integrationof sensory information with assessments of past experience.The LA sends extensive projections to the basal and accessorybasal nuclei and the capsular part of the central nucleus (211,260). Of these, the heaviest projection is to the accessorybasal nucleus. Finally, the lateral nucleus also sends projectionsto the periamygdaloid cortex. Despite early studies suggestingthe contrary (8, 213), all these regions, except the centralnucleus (92), send reciprocal connections back to the LA (248, 249). It is notable that most reciprocal projectionsterminate in the medial and ventrolateral subdivisions in thelateral amygdala, while the dorsolateral subdivision is largelyspared. Furthermore, these reciprocal connections are modestcompared with the lateromedial intranuclear connections. Mostprojections to and from the LA make asymmetrical synapses,indicating they are excitatory (249, 260). However, some ofthe reciprocal connections from the basal nuclei make symmetricalsynapses, suggesting that they are inhibitory (249).
The basal and accessory basal nuclei, which receive strong corticalinputs, have extensive internuclear as well as intranuclearconnections. Within the basal nucleus, all subdivisions haveextensive rostrocaudal connections. The parvicellular subdivisionhas extensive projections to the magnocellular and intermediatesubdivisions (246). The largest projection from basal nucleiis to the medial subdivision of the central nucleus (204, 246, 247). These afferents form asymmetric synapses with spinesand dendrites in the central nucleus and are therefore thoughtto be glutamatergic (204). Because the hypothalamic and brainstem projections from the amygdala responsible for the autonomicresponses of amygdala function largely originate from the medialsubdivision of the central nucleus, these projections fromthe basal nuclei to the central nucleus have a key role incontrolling the output of processed information from the amygdaloidcomplex. The accessory basal nucleus has extensive rostrocaudalconnections and sends afferents to the LA, CeA, and medialdivisions (247).
The central nucleus, which forms a major output of the amygdala,receives inputs from all the other amygdaloid nuclei but sendsvery meager projections back to these nuclei (92). The amygdaloidinputs to the central nucleus are largely restricted to themedial and capsular subdivisions. Within the CeA there areextensive intradivisional and interdivisional connections (92) with each of the four subdivisions making extensive intranuclearconnections. The capsular and lateral subdivision make significantprojections to the medial and capsular subdivisions with alight projection to the intermediate subdivision. The medialdivision largely sends projections out of the amygdala, butalso has a moderate projection to the capsular subdivision(92). It is notable that the lateral subdivision, which formsthe largest projections to the other central subdivisions,receives few reciprocal connections. Interestingly, the lateralsubdivision receives extra-amygdaloid inputs from both corticaland subcortical sources (208), suggesting that this mightalso be a site for integration of inputs to the amygdaloidcomplex.
In summary, there are extensive connections within and betweenthe different nuclei of the amygdaloid complex. These connectionsindicate that there is extensive local processing of informationentering the amygdala before it leads to the appropriate behavioraloutcomes. These intranuclear and internuclear connections havemostly been studied using anatomical tract tracing techniques,coupled in some cases with electron microscopic examinationof the synaptic specializations. However, physiological studiesindicate that amygdala nuclei contain many types of cells thatcannot be readily distinguished on anatomical grounds alone(see below). Furthermore, reconstructed neurons in the lateraland basal nuclei show large dendritic trees, and neurons thathave cell bodies in a particular nuclear subdivision (e.g.,the dorsolateral subdivision of the lateral nucleus) may wellhave dendrites that extend into the next division (e.g., themedial subdivision of the lateral amygdala) (56, 200, 219).This implies that inputs that anatomically terminate in a particularsubdivision of these nuclei may well innervate neurons whosecell bodies are in a different subdivision. Thus the physiologicalimpact of these local connections and their implications forinformation processing remain elusive.