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.

Illustrations-Multiple Memory System

The effects of natural or surgical lesioning certain brain regions and documenting behavioral responses in their absence is one way of discerning human dissociable memory system functions. The following provides a description of the memory retrieval characteristics of amnesiacs to give a conceptualization of how multiple memory systems are represented in the human being and how functional impairments can be behaviorally expressed.

A middle-aged woman in the turn of the century (Claparéde, 1911), in response to Korsakoff’s global amnesia, had only early childhood memory but no intermediate term memory or the ability to remember anything learned in the future. After five years of living in an asylum she did not know where she was and was unable to recognize her doctors and nurses, those with whom she saw and interacted with each and every day. One day her doctor, with whom she had been introduced many times, pricked her hand with a pin. A few hours later he again extended his hand in greeting. In response she pulled her hand away from him. Despite the fact that she was able to associate him with the pinprick, she still had no clear recollection of the event and did not know who he was or his identity. Routine introductions and social discourse were not sufficient to engender memory of individuals and respective social interactions. An uncomfortable pinprick or unconditioned stimulus (US) elicited pain or unconditioned response (UR) that made the owner of the pinprick known (conditioned stimulus-CS) through the painful handshake (conditioned response-CR). This is reflective of intact emotional stimulus-response (amygdala-striatal) learning. The inability for recognizing and/or recalling prior social interactions and personal identity reflects deficits in the structural integrity in either or both hippocampus or thalamus (Kopelman, Lasserson, Kingsley, Bello, Rush, Stanhope et al., 2001; Reed, Lasserson, Marsden, Stanhope, Stevens, Bello et al., 2003; Squire, Haist, & Shimamura, 1989) that typically characterized Korsakoff’s Syndrome.

Another study documented that amnesiacs (typically without a viable MTL region) can acquire the classical conditioned eye-blink, i.e. learn to associate a sensory stimulus (CS) and respond to it (CR) as if it were an uncomfortable (UR) puff of air (US) to the eye. But when subjects were interviewed at the conclusion of a study, they were unable to recall that they had ever participated in the conditioning experiment (Weiskrantz & Warrington, 1979). The ability for acquiring eye blink conditioning or acquisition learning can also be accompanied by the inability for intentional remembering and describing prior experience. This inability for recalling prior experience is also suggestive of hippocampal declarative deficits.

Four memory systems have been noted. Each memory system contributes its part to experience. In each system’s absence learning relating to that region’s function is impaired. Subsequent discussion will elaborate on the characteristics of memory systems.

References

Claparéde, E. (1911). Recognition and selfhood (Subsequently translated by Anne-Marie Bonnel & published in 1995). Consciousness and Cognition, 4(4), 371-8.

Kopelman, M.D., Lasserson, D., Kingsley, D., Bello, R., Rush, C., Stanhope, N., Stevens, T., Goodman, G., Heilpern, G., Kendall, B., & Colchester, A. (2001). Structural MRI volumetric analysis in patients with organic amnesia, 2: correlations with anterograde memory and executive tests in 40 patients. Journal of Neurology and Neurosurgical Psychiatry, 71(1), 23-28.

Reed, L.J., Lasserson, D., Marsden, P., Stanhope, N., Stevens, T., Bello, F., Kingsley, D., Colchester, A., & Kopelman, M.D. (2003). FDG-PET findings in the Wernicke-Korsakoff syndrome. Cortex, 39(4-5), 1027-1045.

Squire, L.R., Haist, F., & Shimamura, A.P. (1989). The neurology of memory: quantitative assessment of retrograde amnesia in two groups of amnesic patients. Journal of Neuroscience, 9(3), 828-839.

Weiskrantz, L., & Warrington, E.K. (1979). Conditioning in amnesic patients. Neuropsychologia, 17, 187-194.