Dissociating space and trace in dorsal and ventral hippocampus

Abstract

Emerging evidence suggests that the hippocampus can be anatomically and functionally dissociated along its septotemporal axis into dorsal and ventral subregions. With respect to function, we have recently demonstrated that pre-training excitotoxic lesions of ventral, but not dorsal, hippocampus impair the acquisition of trace fear conditioning, whereas post-training lesions of either dorsal or ventral hippocampus impair the subsequent expression of trace fear conditioning (Yoon and Otto (2007) Neurobiol Learn Mem 87:464-475). In addition to trace fear conditioning, dorsal and ventral hippocampus appear to be differentially involved in a number of spatial memory tasks. The present study examined the effects of temporary inactivation of dorsal or ventral hippocampus on the acquisition and expression of trace fear conditioning and on performance of a spatial delayed reinforced alternation task. The findings demonstrate a double dissociation of dorsal and ventral hippocampal function: inactivation of ventral, but not dorsal, hippocampus attenuated the acquisition and expression of trace fear conditioning, whereas inactivation of dorsal, but not ventral, hippocampus dramatically impaired performance in the delayed reinforced alternation task. These data further support the notion that dorsal and ventral hippocampus contribute differentially to performance in a variety of paradigms.

Time course of dorsal and ventral hippocampal involvement in the expression of trace fear conditioning

“…Conversely VH, but not DH, establishes direct and reciprocal connections with the amygdala (Pitkanen et al, 2000), a brain area known to play a prominent role in emotional learning and anxiety states (LeDoux, 1995). Consistent with these neuroanatomical dissociations, we have recently reported a double dissociation between VH and DH in the acquisition and expression of auditory trace fear conditioning and spatial learning, respectively (Czerniawski et al, 2009;Czerniawski et al, 2011;Yoon & Otto, 2007). Collectively, these data suggest that the dorsal and ventral hippocampal subregions may contribute differently to the acquisition and subsequent expression of a variety of mnemonic processes, and that the apparently discrepant data reviewed above may reflect functional differences between DH and VH.…”

“…First, most studies exploring the role of the hippocampus in systems consolidation have examined the effects of damage to either the majority of the hippocampal formation or selective damage to the dorsal hippocampus (DH) alone (see Sutherland et al, 2010 for review). By contrast, relatively few studies have selectively examined the contributions of the ventral hippocampus (VH) to recall in general and systems consolidation in particular (Czerniawski et al, 2009;Martin et al, 2005;Sutherland et al, 2008;Yoon & Otto, 2007). While DH and VH are extensively interconnected, these subdivisions receive notably different afferents and, moreover, the roles associated with the sources of these afferents are consistent with recent data demonstrating the dissociable roles of DH and VH in different forms of learning.…”

“…The infusion methods used in the present study were identical to those used previously in our laboratory (Czerniawski et al, 2009;, 2010.…”

“…Trace and delay conditioning paradigms were similar to those used previously in our laboratory (Czerniawski et al, 2009). Briefly, conditioning in both paradigms took place in a single session consisting of 10 pairings of an explicit auditory stimulus (CS) (20 sec, 3.9 kHZ, 80 db) with scrambled footshock (US) (2 sec, 0.6 mA).…”

“…While DH and VH are extensively interconnected, these subdivisions receive notably different afferents and, moreover, the roles associated with the sources of these afferents are consistent with recent data demonstrating the dissociable roles of DH and VH in different forms of learning. Specifically, DH receives substantially denser sensory projections from the entorhinal cortex than VH (Pitkanen et al, 2000), and is critical for spatial learning (Czerniawski et al, 2009;Moser & Moser, 1998). Conversely VH, but not DH, establishes direct and reciprocal connections with the amygdala (Pitkanen et al, 2000), a brain area known to play a prominent role in emotional learning and anxiety states (LeDoux, 1995).…”