Basolateral amygdala projections to ventral hippocampus modulate the consolidation of footshock, but not contextual, learning in rats

Abstract

The basolateral amygdala (BLA) modulates memory consolidation for a variety of types of learning, whereas other brain regions play more selective roles in specific kinds of learning suggesting a role for differential consolidation via distinct BLA pathways. The ventral hippocampus (VH), an efferent target of the BLA, has been suggested to selectively process emotionrelated learning, yet whether the BLA VH pathway modulates memory consolidation, and does so in a learning-specific manner, is unknown. To address this issue, the BLA of male Sprague-Dawley rats was bilaterally transduced to express either ChR2(E123A) or eArchT3.0. Fiber optic probes were implanted in the VH to provide illumination of BLA axons. Rats then underwent a modified contextual fear conditioning task permitting separation of context and footshock learning. On day 1, rats received 3 min of pre-exposure to the apparatus. On day 2, rats were placed into the apparatus, received an immediate footshock, and quickly removed. Retention was tested on day 4. Optical stimulation of the BLA VH pathway following footshock, but not context, training using trains of 40-Hz light pulses enhanced retention. Continuous optical inhibition of this pathway for 15 min starting 25 min after footshock training impaired retention. These findings indicate that BLA VH projections influence the consolidation for footshock, but not context, learning of a modified CFC task and provide direct evidence that BLA projections to other brain regions modulate memory consolidation selectively depending on the kind of learning involved.Learning and memory involves complex interactions among multiple brain regions that play discrete roles in the consolidation of specific kinds of memories. However, work strongly indicates that the basolateral amygdala (BLA) modulates the consolidation of a wide array of memories. It has been hypothesized that the BLA plays this more general role, at least in part, through interactions with distinct regions (McGaugh 2002(McGaugh , 2004McIntyre et al. 2012). BLA connections with forebrain regions such as the hippocampus and striatum that are selectively involved in the consolidation of certain kinds of memories (McDonald 1991;Pitkänen et al. 2000;McGaugh 2002;Malin and McGaugh 2006;Paz et al. 2006;Chavez et al. 2013) suggest that efferent pathways from the BLA may be selectively involved in modulating consolidation for specific kinds of information.Indeed, much evidence suggests that the BLA interacts with the hippocampus during memory consolidation (Packard et al. 1994;Roozendaal et al. 1999;Malin and McGaugh 2006) and that the BLA directly or indirectly influences activity and plasticity in different parts of the hippocampal formation (Ikegaya et al. 1995;Frey et al. 2001;McIntyre et al. 2005;McReynolds et al. 2014;Lovitz and Thompson 2015). These findings suggest pathway mechanisms by which the BLA influences the consolidation of memories regulated by the hippocampal formation. However, the hippocampus comprises different subregions, including dors...

The anterior medial temporal lobes: Their role in food intake and body weight regulation

“…The nature of the interactions between the amygdala and hippocampus may consequently vary in different sub-parts of these structures and underlie different functions. In line with this notion, Huff, Emmons, Narayanan, & LaLumiere [68] have shown that the basolateral amygdala interacts with the ventral hippocampus to modulate specific types of learning (e.g., footshock learning) but not others (here context learning). This is also suggests that similarly, the hippocampus may not be one entity (e.g., [36,53,85,101]).…”

Attenuation of cocaine seeking in rats via enhancement of infralimbic cortical activity using stable step-function opsins

“…This SSFO-mediated current has been suggested to enhance activity in a structure without directly driving action potential patterns (Liu et al 2016; Yizhar et al 2011a; Yizhar et al 2011b). This represents a significant advantage over the use of traditional ChR2 constructs, which require the identification of stimulation parameters to drive neuronal activity in behaviorally relevant ways, a process that can necessitate a large number of experiments and varies depending on brain region or behavior under study (Huff et al 2016; Huff et al 2013). SSFOs also represent an advantage over DREADD approaches, as SSFOs can be activated with one wavelength of light, and deactivated with another, increasing temporal control over the manipulation.…”

Bridging the Gap : Towards a cell-type specific understanding of neural circuits underlying fear behaviors

“…Interestingly, activation of these projections following contextual training had no effect upon fear memory; however, activation following foot-shock enhanced fear learning. This suggests that afferents from BLA to vHPC may be primarily involved in encoding aversive, but not contextual elements of fear conditioning 65 .…”

“…Additional evidence that target specific projections from the BLA may play a role in the consolidation of select types of memory comes from Huff et al (2016). The authors activated or inhibited projections from the BLA to the vHPC during a modified contextual freezing conditioning task so as to determine whether these projections are necessary for encoding context or foot-shock memory.…”