Multiple Memory Systems-Triple Dissociation
Memory loss or amnesia can best be understood within the context of a loss of function of one of many dissociable memory systems that characterize the brain. Each memory system contributes certain elements of experience that in total represent a single experience. Some of these elements operate outside awareness in forming memories for habits or procedures or emotional responses that attract or repel one from interacting with others. Subsequent discussion will elaborate on multiple memory systems within the context of neuroscience research. This discussion will help to later identify how the loss of integrity of one memory system, declarative memory system, underlies impairments in retrieval of memory and possibly underlie impairments in later trauma retrieval.
The presence of multiple memory systems and parallel learning has also been supported in recent neuroscience animal research. Triple (McDonald & White, 1993, 1995) and double (Chai & White, 2004) dissociation methods have been very effective at holding factors constant for illustrating different contributions of parallel memory systems during specific tasks. For example four memory systems, the hippocampal region, dorsal striatal, sensory cortex and amygdala, have been identified. Each has different connections, interactions, and receives different information from different brain structures. Each powerfully influences and uniquely contributes to discrete behavioral expression (White & McDonald, 2002). Removing a specific area of the hippocampal region demonstrates that it is needed for informational processing about changing relationships among environmental cues and for resolving feature ambiguity in place or spatial location (McDonald, Murphy, Guarraci, Gortler, White, & Baker, 1997). The hippocampal area is also needed for facilitating stimulus-stimulus (S, S*) relational learning that represents relationships between and among different stimuli (White & McDonald, 2002). In its absence, learning is slowed (McDonald & White, 1995). To compensate for its loss, the animal relies on exteroceptive input from the sensory cortex to learn about perceptual features in the environment (Badgaiyan & Posner, 1997). The animal also relies on the use of the dorsal striatal-caudate motor system’s egocentric information and self generated movement to learn about the environment. (DeCoteau & Kessner, 2000; Kesner, Bolland, & Dakis, 1993). Both of these memory systems are necessary for simple stimulus-response (S-R) learning and in their absence related task acquisition is impaired (White & McDonald, 2002). On the other hand neural inactivation of the striatal region allows for hippocampal expression of place learning, which is the tendency for retrieving previously learned behavioral sequences (DeCoteau & Kessner, 2000; Packard & McGaugh, 1996). In the adult one memory system may substitute for another in its absence to meet task dependent criteria (Squire, 2004).
Another memory system involves the amygdala. The amygdala in interaction with the ventral striatum plays a key role in identifying anticipated cues that had been associated with rewarding (or aversive) outcomes. It identifies and resolves cue ambiguity by identifying biologically salient stimuli in passive place learning (McDonald & White, 1995). The amygdala-ventral striatal system works closely with other memory systems to modulate response selection for approach or avoidance according to reward or aversion magnitude respectively (Chai & White, 2004; Holahan & White, 2002). These memory systems in interaction with each other and in their relationship with the prefrontal cortex are represented in the memory classification systems noted in subsequent sections (Atallah, Frank, & O’Reilly, 2004). Each memory system has a temporally determined contribution depending upon task-related demands (Poldrack & Rodriguez, 2004). Each memory system’s absence allows for expression of the other memory systems. Any compensatory response by expressed regions will be limited by their regional functional specialization.
References
Atallah, H.E., Frank, M.J., & O’Reilly, R.C. (2004). Hippocampus, cortex, and basal ganglia: insights from computational models of complementary learning systems. Neurobiological Learning and Memory, 82(3), 253-267.
Badgaiyan, R.D., & Posner, M.I. (1997). Time course of cortical activations in implicit and explicit recall. Journal of Neuroscience, 17(12), 4904-13.
Chai, S.C., & White, N.M. (2004). Effects of fimbria-fornix, hippocampus, and amygdala lesions on discrimination between proximal locations. Behavioral Neuroscience, 118(4), 770-784.
DeCoteau, W.E., & Kesner, R.P. (2000). A double dissociation between the rat hippocampus and medial caudoputamen in processing two forms of knowledge. Behavioral Neuroscience, 114(6), 1096-1108.
Holahan, M.R., & White, N.M. (2002). Conditioned memory modulation, freezing, and avoidance as measures of amygdala-mediated conditioned fear. Neurobiology of Learning and Memory, 77(2), 250-275.
Kesner, R.P., Bolland, B.L., & Dakis, M. (1993). Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Experimental Brain Research, 93(3), 462-470.
McDonald, R.J., Murphy, R.A., Guarraci, F.A., Gortler, J.R., White, N.M., & Baker, A.G. (1997). Systematic comparison of the effects of hippocampal and fornix-fimbria lesions on acquisition of three configural discriminations. Hippocampus, 7(4), 371-388.
McDonald, R.J., & White, N.M. (1993). A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behavioral Neuroscience, 107(1), 3-22.
McDonald, R.J., & White, N.M. (1995). Hippocampal and nonhippocampal contributions to place learning in rats. Behavioral Neuroscience, 109(4), 579-593.
Packard, M.G., & McGaugh, J.L. (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory, 65(1), 65-72.
Poldrack, R.A., & Rodriguez, P. (2004). How do memory systems interact? Evidence from human classification learning. Neurobiology of Learning and Memory, 82(3), 324-332.
Squire, L.R. (2004). Memory systems of the brain: a brief history and current perspective. Neurobiology of Learning and Memory, 82(3), 171-7.
White, N.M., & McDonald, R.J. (2002). Multiple parallel memory systems in the brain of the rat. Neurobiology of Learning and Memory, 777, 125-184.