Neurons in the lateral and basolateral nuclei of the rat amygdala were studied using Golgi-Kopsch and rapid Golgi techniques. According to differences in perikaryal, dendritic, and axonal morphology, three main neuronal classes are recognized. Class I neurons, the predominant cell type in both nuclei, are large, spiny neurons that vary in size in different subdivisions of the lateral and basolateral nuclei. These neurons often have a pyramidal shape, exhibiting one or two thick "apical" dendrites and several thinner "basal" dendrites. Axons of class I neurons, which appear to pass out of the nucleus of origin, usually give off several collaterals that arborize modestly in the vicinity of the cell. Class II neurons are smaller, ovoid cells that comprise approximately 5% of impregnated neurons. These neurons are characterized by spine-sparse dendrites and fairly dense local axonal arborizations. Class II neurons may be classified as multipolar, bitufted, or bipolar, depending on dendritic branching pattern. Another type of class II neuron, the amygdaloid chandelier cell, is recognized by virtue of its distinctive axon. The chandelier cell axon gives off numerous collaterals that form nestlike entanglements exhibiting clusters of axonal varicosities. Isolated chandelierlike axons of undetermined origin were observed forming multiple contacts with initial segments of class I axons. Several small, spherical class III neurons with short, varicose dendrites were observed. Axons branch profusely to form a dense tangle of collaterals in the vicinity of the cell. Both axons and dendrites establish numerous contacts with class I dendrites. This investigation, the first detailed Golgi study of the basolateral amygdala of the rat, reveals that the cytoarchitecture of this brain region in the rat is basically similar to that of the opossum and other mammals. Morphologic details described in this report should be useful in the interpretation of ultrastructural, immunocytochemical, and electrophysiological studies of the basolateral amygdala.
The generation of emotional responses by the basolateral amygdala is largely determined by the balance of excitatory and inhibitory inputs to its principal neurons, the pyramidal cells. The activity of these neurons is tightly controlled by GABAergic interneurons, especially a parvalbumin-positive (PV+) subpopulation that constitutes almost half of all interneurons in the basolateral amygdala. In the present semi-quantitative investigation we studied the incidence of synaptic inputs of PV+ axon terminals onto pyramidal neurons in the rat basolateral nucleus (BLa). Pyramidal cells were identified using calcium/calmodulin-dependent protein kinase II (CaMK) immunoreactivity as a marker. In order to appreciate the relative abundance of PV+ inputs compared to excitatory inputs and other non-PV+ inhibitory inputs, we also analyzed the proportions of asymmetrical (presumed excitatory) synapses and symmetrical (presumed inhibitory) synapses formed by unlabeled axon terminals targeting pyramidal neurons. The results indicate that the perisomatic region of pyramidal cells is innervated almost entirely by symmetrical synapses, whereas the density of asymmetrical synapses increases as one proceeds from thicker proximal dendritic shafts to thinner distal dendritic shafts. The great majority of synapses with dendritic spines are asymmetrical. PV+ axon terminals mainly form symmetrical synapses. These PV+ synapses constitute slightly more than half of the symmetrical synapses formed with each postsynaptic compartment of BLa pyramidal cells. These data indicate that the synaptology of basolateral amygdalar pyramidal cells is remarkably similar to that of cortical pyramidal cells, and that PV+ interneurons provide a robust inhibition of both the perisomatic and distal dendritic domains of these principal neurons. Keywordsimmunocytochemistry; electron microscopy; inhibition, calcium/calmodulin-protein kinase II The basolateral amygdala (ABL), which consists of the lateral, basolateral, and basomedial amygdalar nuclei, is one of the most important brain regions for the generation of emotional behavior and the formation of emotional memories (Aggleton, 1992;Aggleton, 2000;Shinnick-Gallagher et al., 2003). It receives sensory information from the thalamus and cerebral cortex (McDonald, 1998) and produces appropriate emotional responses by activating a variety of subcortical regions including the central amygdalar nucleus, bed nucleus of the stria terminalis, and striatum. The outputs of the ABL arise from pyramidal cells (McDonald, 1992b), which resemble their counterparts in the cerebral cortex. These neurons, which constitute about 85% of the neurons in the ABL, are characterized by a pyramidal or piriform cell body, and spiny dendrites (Hall, 1972;McDonald, 1982McDonald, , 1984 1992a,b;Millhouse and DeOlmos, 1983). Some ABL pyramidal cells have a marked pyramidal morphology, with a clear differentiation of thicker "apical" dendrites from thinner "basal" dendrites, whereas others have a semipyramidal or even stellate appe...
Since recent studies indicate that distinct neuropeptides and projections are associated with discrete portions of the central amygdaloid nucleus (CN), a detailed investigation of the cytoarchitecture of CN should contribute to an understanding of its organization. Qualitative and quantitative analyses of the rat CN using Nissl, Klüver-Barrera, and Golgi techniques suggests that it consists of four subdivisions. The medial subdivision (CM), which is closely associated with the stria terminalis, is narrow caudally but enlarges near the rostral pole of CN. Most neurons in CM have long dendrites that branch sparingly and have a moderate number of dendritic spines. A smaller number of CM neurons have thick dendrites with virtually no spines. Lateral to CM is the lateral subdivision (CL) which appears round in coronal sections. Neurons of CL have a very dense covering of dendritic spines and resemble medium-size spiny neurons of the striatum. Area X of Hall contains spiny neurons similar to those of CL and spine-sparse neurons that resemble medium-size spine-sparse cells of the striatum. Since area X encapsulates the lateral aspect of CL, it is termed the lateral capsular subdivision (CLC) of CN. The lateral capsular subdivision enlarges rostrally and is divided into dorsal and ventral portions by a laminar extension of the putamen. Near the rostral pole of CN a small region of tightly packed, intensely stained neurons is interposed between CL and CM. Golgi preparations reveal that this intermediate subdivision (CI) of CN contains neurons similar to those of CM. The lateral subdivision, CLC, and CM correspond, in part, to subdivisions recognized in previous Nissl studies. The intermediate subdivision has not been recognized as a distinct subdivision in previous investigations. This is the first Golgi study to recognize differences in neuronal morphology in particular subdivisions of the rat CN. The correlation of Nissl and Golgi preparations has permitted a more accurate determination of the boundaries and total extent of each subdivision than the use of Nissl techniques alone.
Summary Activation of corticotrophin releasing factor (CRF) neurons in the paraventricular nucleus of the hypothalamus (PVN) is necessary for establishing the classic endocrine response to stress, while activation of forebrain CRF neurons mediates affective components of the stress response. Previous studies have reported that mRNA for CRF2 receptor (CRFR2) is expressed in the bed nucleus of the stria terminalis (BNST) as well as hypothalamic nuclei, but little is known about the localization and cellular distribution of CRFR2 in these regions. Using immunofluorescence with confocal microscopy, as well as electron microscopy, we demonstrate that in the BNST CRFR2-immunoreactive fibers represent moderate to strong labeling on axons terminals. Dual-immunofluorescence demonstrated that CRFR2-fibers co-localize oxytocin (OT), but not arginine-vasopressin (AVP), and make perisomatic contacts with CRF neurons. Dual-immunofluorescence and single cell RT-PCR demonstrate that in the hypothalamus, CRFR2 immunoreactivity and mRNA are found in OT, but not in CRF or AVP-neurons. Furthermore, CRF neurons of the PVN and BNST express mRNA for the oxytocin receptor, while the majority of OT/CRFR2 neurons in the hypothalamus do not. Finally, using adenoviral-based anterograde tracing of PVN neurons, we show that OT/CRFR2-immunoreactive fibers observed in the BNST originate in the PVN. Our results strongly suggest that CRFR2 located on oxytocinergic neurons and axon terminals might regulate the release of this neuropeptide and hence might be a crucial part of potential feedback loop between the hypothalamic oxytocin system and the forebrain CRF system that could significantly impact affective and social behaviors, in particular during times of stress.
The projections of the cerebral cortex to the extended amygdala were studied in the rat using anterograde and retrograde tract-tracing techniques. Most cortical areas with strong projections to the extended amygdala preferentially targeted either the medial extended amygdala (including the medial amygdalar nucleus, ventromedial substantia innominata, and the medial part of the bed nucleus the stria terminalis) or the central extended amygdala (including the central amygdalar nucleus, dorsolateral substantia innominata, and the lateral part of the bed nucleus of the stria terminalis). Some cortical areas, however, had equal projections to both medial and central portions. The main areas projecting preferentially to the medial extended amygdala were the ventral subiculum, infralimbic cortex, ventral agranular insular area, and the rostral part of the ventrolateral entorhinal area. The main areas projecting preferentially to the central extended amygdala were the prefrontal cortex, viscerosensory and somatosensory portions of the insular cortex, and the amygdalopiriform transitional area. It is suggested that these cortical inputs may be important for cognitive, mnemonic, and affective aspects of emotional and motivated behavior.
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