Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes.

Abstract

These experiments investigated the effects, on memory, of injections of d-amphetamine (10 pg/0.5 id) adminitered into the amygdala, hippocampus, or caudate nucleus immediately after traning in cued or spatial water-maze tasks. In experiment 1, rats received an eight-trial training session on one of the two tasks followed by injections of d-amphetamlne or saline. The amygdala is known to project to both the hippocampus and caudate nucleus (17)(18)(19)(20), and the finding that c-fos is expressed in hippocampus and caudate nucleus following intraamygdala injections of the excitatory amino acid N-methyl-D-aspartate (21) indicates that the amygdala is functionally connected with both of these structures. Such evidence suggests the possibility that the amygdala may influence both hippocampal-and caudate-dependent memory.To investigate this implication, experiment 1 examined the effects of posttraining intraamygdala injections of d-amphetamine on memory for two different types of water-maze tasks-a spatial task and a cued task-that are known to differentially involve the hippocampus and caudate nucleus, respectively (4, 22, 23). d-Amphetamine was used in these experiments because of extensive evidence that d-amphetamine enhances retention of a variety of tasks when administered either centrally (5, 24) or peripherally (25,26).In the spatial task, rats were trained to swim to an escape platform placed in a constant spatial location. As the top of the platform was 1.0 cm below the water surface, and rats were trained to approach the platform from different start points, the platform could be located only by learning spatial relationships among distal extramaze cues. In the cued task, rats were trained to swim to a visible cue mounted on a platform, which was placed in a different spatial location on each trial.Experiment 2 was designed to determine whether the amygdala was involved as a locus of changes mediating the amygdala influences on memory in these two tasks. Rats were trained on one of the two tasks, given posttraining intraamygdala injections of d-amphetamine or saline, and then, shortly before testing, given an intraamygdala injection of lidocaine to inactivate the amygdala. Apparatus. The water maze was a black circular galvanized steel tank (diameter, 1.83 m; height, 0.58 m) filled with water (250C) to a depth of 20 cm. Four starting positions (north, south, east, west) were equally spaced around the perimeter of the tank, dividing the pool into quadrants. The rectangular Plexiglas escape platform used for the spatial task (11 x 14 x 19 cm) was submerged at a depth of 1 cm. For the cued task, a black and white striped rubber ball (diameter, 8 cm) was attached to the top of the submerged platform and protruded above the water surface. The platform could be used as a step to mount the ball and escape the water. MATERIALS AND METHODSSurgery. Animals were anesthetized with sodium pentobarbital (50 mg/kg). Unilateral guide cannulae were implanted on the left side by standard stereotaxic techniques. For th...

Amygdala activity at encoding correlated with long-term, free recall of emotional information.

“…Several studies now suggest that the left prefrontal cortex is more involved with memory storage processes, and *' * ' that the right prefrontal cortex is more important for memory 6 0.7 0.8 retrieval (37,38). Consistent with this notion of asymmetrical lucose function, stimulation of the left AC alone is sufficient to modulate memory storage in rats (41), whereas the right AC in rats appears more involved than the left with memory retrieval (42). Furthermore, a recent PET study implicates the ssion right AC in retrieval of affect-laden autobiographical memories ( (35) report that activity in several brain regions (e.g., the right cerebellar deep nuclei) correlated significantly with degree of learning despite the fact that the training and control conditions did not produce different overall glucose levels in these regions.…”

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

“…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.…”

“…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, evidence also indicates that different types or kinds of learning involve separate and distinct brain regions, as, for example, the hippocampus and caudate are involved in the consolidation of spatial and cued water maze learning, respectively (Packard et al 1994). The BLA interacts with a variety of structures both cortical (e.g., anterior cingulate cortex, insular cortex) and subcortical (e.g., caudate, nucleus accumbens) during memory consolidation, potentially accounting for its diffuse involvement in consolidation across tasks and types of memory (for recent review, see McIntyre et al 2012).…”

“…Prior studies indicate that the BLA modulates the consolidation for many different types of learning including inhibitory avoidance (LaLumiere et al 2004(LaLumiere et al , 2005, CFC Huff and Rudy 2004), conditioned taste aversion (Miranda et al 2003;Guzman-Ramos and Bermudez-Rattoni 2012), spatial and cued-response learning (Packard et al 1994), and novel object recognition (Roozendaal et al 2008;Bass et al 2012). However, evidence also indicates that different types or kinds of learning involve separate and distinct brain regions, as, for example, the hippocampus and caudate are involved in the consolidation of spatial and cued water maze learning, respectively (Packard et al 1994).…”