Hippocampal and amygdaloid interactions in the nucleus accumbens

Abstract

The nucleus accumbens, in view of its afferent and efferent fiber connections, appears to hold a key position for "limbic" (e.g., hippocampal and amygdaloid) influences to reach somatomotor and autonomic brain structures, and it has therefore been considered as a limbic-motor interface. The nucleus accumbens can be subdivided into a shell and a core region, which both contain further inhomogeneities. The present account first summarizes the detailed topographical anatomical relationships of inputs from different dorso-ventral parts of the hippocampus and different rostrocaudal parts of the basal amygdaloid complex at the level of the accumbens. Subsequently, the electrophysiological characteristics of hippocampal and amygdaloid inputs in the accumbens are described. Interactions between hippocampal and amygdaloid inputs appear to exist primarily in the medial parts of both the shell and the core of the nucleus accumbens. In the short term, stimulating amygdaloid inputs appear to facilitate hippocampal throughput (heterosynaptic paired pulse facilitation), whereas stimulation of hippocampal inputs depresses amygdaloid throughput in a paired pulse paradigm. Tetanic stimulation of hippocampal inputs to the accumbens leads to a decrementallong-term potentiation (LTP) of this fiber pathway (homosynaptic LTP) but, along a similar time range, to a depression of amygdaloid inputs (heterosynaptic long-term depression). The involvement of dopaminergic, GABAergic, and glutamatergic mechanisms in these interactions is discussed. Finally, it is suggested that the interactions between hippocampal and amygdaloid inputs at the level of the nucleus accumbens playa role in different aspects of associative learning.

A differential involvement of the shell and core subterritories of the nucleus accumbens of the rats in memory processes.

“…It is important to note that, in view of the converging anatomical connections with both the amygdala and hippocampus (Groenewegen et al, 1987; Groenewegen, Mulder, et al, 1999; Groenewegen, Wright, et al, 1999), it is unlikely that the nucleus accumbens, and in particular its shell subterritory, would play a more prominent role in contextual conditioning only, instead of being involved in conditioning both to the context and to the CS, as is the case with the amygdala and the ventral hippocampus (Bast et al, 2001; Campeau & Davis, 1995; Campeau, Miserendino, & Davis, 1992; Kim & Fanselow, 1992; Maren, 1999; Maren, Aharonov, Stote, & Fanselow, 1996; Maren & Fanselow, 1995; R. G. Phillips & LeDoux, 1992; Richmond et al, 1999; Zhang et al, 2001).…”

“…The nucleus accumbens is a rather complex and heterogeneous structure composed of two neurochemically distinct major subterritories: a central core region and a more peripherally located shell region (Jongen-Rêlo, Voorn, & Groenewegen, 1994; Meredith, Agolia, Arts, Groenewegen, & Zahm, 1992; Voorn, Gerfen, & Groenewegen, 1989; Zaborszky et al, 1985; Zahm & Brog, 1992). This bi-partition of the nucleus accumbens also holds for the distribution of the various inputs and outputs of the nucleus (Berendse, Galis-de Graaf, & Groenewegen, 1992; Berendse, Groenewegen, & Lohman, 1992; Groenewegen et al, 1999; Groenewegen, Wright, & Beijer, 1996; Groenewegen, Wright, Beijer, & Voorn, 1999; Heimer et al, 1997; Heimer, Zahm, Churchill, Kalivas, & Wohltmann, 1991; Zahm & Brog, 1992; Zahm & Heimer, 1990). In a general view, whereas the shell is predominantly innervated by limbic structures, the core is believed to be a ventral extension of the dorsal striatum (Alheid & Heimer, 1996; Zahm & Heimer, 1990).…”

Neurobehavioral foundation of environmental reactivity.

“…DA release in the NAc additionally facilitates the creation of associations between rewards and stimuli that predict those rewards (i.e., conditioned stimuli; Montague, Hyman, & Cohen, 2004;Schultz, 1997Schultz, , 2007. Corticolimbic inputs originating from perceptual processing pathways and areas that compute the incentive salience of contextual stimuli (i.e., the basolateral amygdala [BLA], medial orbital frontal cortex [mOFC], and extended amygdala) converge on the NAc with VTA DA inputs to facilitate binding of an ensemble of the incentive value of a stimulus and its associated context (Berke & Hyman, 2000;Depue & Morrone-Strupinsky, 2005;Groenewegen et al, 1999;Groenwegen, Wright, Beijer, & Voorn, 1999;O'Donnell, 1999). That ensemble is further compressed in a cortico-cortical loop, which terminates in the mOFC where the ensemble is associated with an expected outcome (i.e., probability and magnitude of reward; Alexander & Crutcher, 1990;Amodio & Frith, 2006;O'Donnell, 1999).…”

Ventral subiculum inputs to nucleus accumbens medial shell preferentially innervate D2R medium spiny neurons and contain calcium permeable AMPARs

“…We then performed dual whole cell recordings in ex vivo slices of nearby TdTomato + (D1R) and TdTomato − (putative D2R) MSNs in dorsal NAcMS and performed terminal stimulation to measure light-evoked excitatory postsynaptic currents (EPSCs). As vSUB fiber density varies along the rostral-caudal axis of NAcMS (Groenewegen et al, 1999), recording from neighboring pairs of D1R and D2R MSNs allows for the direct comparison of vSUB input to D1R vs D2R MSNs. We first sought to characterize the relative strengths of vSUB-D1R and vSUB-D2R MSN excitatory synapses by assessing the input-output (I/O) relationship.…”