Implicit-Nondeclarative Memory

Freud attributed unconscious processes and repression to deficits in the ability for remembering (Erdelyi, 1985). There are, however, many different reasons for memory impairment. Memory loss has been traced to deficits in two aspects declarative and explicit memory (Schacter, 1992; Squire, 1992). Declarative memory is the cognitive ability for declaring and bringing to mind remembered images and their relationships. Awareness is dependent on the latter. Deliberate memory impairment has been associated with the expression of two elements, nondeclarative and implicit memory. Both are expressed during behaviors necessitating perceptual-motor and habit memory, behaviors that do not involve intentional retrieval or recall (Schacter, 1992; Squire, 1992). Either aspect or element will represent its respective memory process during subsequent discussion and will be used interchangeably.

Implicit or nondeclarative memory is memory that has been learned without phenomenal awareness and “pops into mind” as illustrated earlier (Schacter, 1987). It is also characterized as inaccessible and not recallable (Roediger, 1990). It is data driven. It is guided by immediate task-related information that does not require conceptual recall. It is inflexible, i.e. insensitive to surface perceptual changes and exclusively linked to the original learning context (Schacter, 1990). Learning underlying the expression of implicit memory is also slowly acquired. Its learning is gradual, incremental and requires many trials (Squire, 1992). Due to its persistence and enduring quality, this type of memory requires many trials for unlearning. Implicit memory’s expression is also behaviorally inferred (Squire, 1992) and modality specific, i.e. associated with one motor or sensory modality. It is characterized by the formation of simple feature associations and conditioning processes, including classical conditioning and emotional learning (Squire, Knowlton, & Musen, 1993). Finally implicit memory is also associated with corticostriatal response or stimulus-response learning. One example of implicit learning is perceptual priming, which is the data driven task ability for identifying and matching sensory fragments to a whole item (Eichenbaum, 2002). Another example is procedural memory, which is the ability for learning motor sequences that are inherent in skill-learning (Ryan & Cohen, 2003). In summary nondeclarative-implicit memory is behaviorally inferred and inflexible. It is characterized as slow learning and as requiring many trials to meet performance demands.

Different brain regions are involved in task-dependent implicit processing. According to neuroimaging findings increased activations in cortical and/or striatal areas coupled with concomitant decreases in corticohippocampal regions characterize implicit sensorimotor learning like finger movement sequencing (Bischoff-Grethe, Goedert, Willingham, & Grafton, 2004) or perceptual priming (Schott, Henson, Richardson-Klavehn, Becker, Thoma, Heinze et al., 2005). Depending upon the task, visual object priming tasks can either activate posterior cortical sensory occipitoparietal (visual and somatosensory) regions in concert with the dorsolateral prefrontal and frontal cortex (Badgaiyan & Posner, 1997; James, Humphrey, Gati, Menon, & Goodale, 2000) or deactivate portions of the fusiform gyrus, medial occipital cortex, inferior frontal gyrus, and medial temporal lobe structures (Schott et al., 2005). Incidental categorical learning, i.e. identifying a perceptual object, the middle dot of five on a computer screen, reduces activity in the extrastriate-occipital visual cortex (Reber, Gitelman, Parrish, & Mesulam, 2003; Schacter, Alpert, Savage, Rauch, & Albert, 1996). Serial reaction time (SRT) is an implicit task, which requires pressing a button in response to a target’s appearance in one of four different horizontal locations. The SRT task has been shown to activate a region in the parietal lobe, a prefrontal region called the inferior mid-frontal gyrus, and the striatum’s caudate nucleus and putamen (Willingham, Salidis, & Gabrieli, 2002; Rauch, Whalen, Savage, Curran, Kendrick, Brown, Bush, et al., 1997; Peigneux, Maquet, Meulemans, Destrebecqz, Laureys, Degueldre, et al., 2000) with concomitant decreases in the thalamus (Rauch, Walen, Curran, McInerney, Heckers, & Savage, 1998). Accordingly perceptual motor implicit memory appears to be associated with corticostriatal interactions.

Amnesiacs, individuals having suffered damage to the MTL, have been found to possess fully intact implicit perceptual memory for having performed a verbal repetition task called semantic priming (Hamann & Squire, 1997). Various cues or hints are needed to support later task-related recognition and recollection (Schacter, 1994). An amnesiac with MTL damage, H.M., was unimpaired in his completion of sorting, perceptual, and face-perception tasks and a hidden-figures test. He was however impaired in performing tasks with delays greater than five seconds (Milner, 1972) and in retrospective remembering of ever having performed the task before (Milner, Corkin, & Teuber, 1968). Both these deficits suggest impairments in retention and retrieval (Pigott & Milner, 1993). H.M. also suffered significant temporally graded retrograde amnesia for autobiographical memory and facts and anterograde amnesia for newly learned experiences and facts (Milner et al., 1968). He was also unable to recognize and remember recently introduced close neighbors and family friends. H.M. forgot their identities and names. This necessitated repeated introductions. However, H.M. had intact long-term memory of early episodes during childhood and could recognize and knew his parents.

Within this conceptualization, classical eye blink, reward, and fear conditioning paradigms are also considered to be implicit because they satisfy most of the characteristics that represent it noted above (Squire, 2004). Conditioning transpires when a benign stimulus, the conditioned stimulus (CS), takes on the respective pleasant/unpleasant and rewarding/painful stimulus qualities of the unconditioned stimulus (US). With successful pairing, the CS is able to produce a conditioned response (CR) that is reminiscent of the unconditioned response (UR) to the US (Pavlov, 1927). Evidence of conditioned behavior, conditioned response (CR), is inferred through conditioned eye blink, reward mediating approach behaviors, and startle and fearful behaviors of freezing and avoidance to a CS. Conditioning is data driven, as both US and/or CS need to be present in order to produce targeted and recognized unconditioned or conditioned responses respectively. CS-CR learning needs to be inextricably tied to the original learning context due to the CS’s relationship with the US; either needs to be present to elicit an UR or CR. (The CS acts like a cue or hint to support conditioning task-related recognition and recollection as a prime in semantic-priming.) Conditioning learning and memory also share stimulus-response processing style with implicit learning (White & McDonald, 2002). It is persistent and enduring because without unpairing and extinction processes the CR persists in the presence of the CS. Moreover, it is not sufficient to allow only time to pass to extinguish this association. Repeated reexposure of the unpaired and nonreinforced CS is necessary over many sessions for extinction to occur (Garcia, 2002; Pavlov, 1927). Because conditioning involves the acquisition of new associations, it is relatively slow learning when compared with one trial declarative learning (Squire, 1992). Reward conditioning in the rodent needs four daily ten minute trials (Peinado-Manzano, 1988). Moreover, trace fear conditioning needs seven 10 second tone-shock temporal linkages within an eighteen minute session to meet conditioning criteria (Runyan, Moore, & Dash, 2004). Finally emotional conditioning can be differentiated from other types of implicit memory in its associating different multiple sensory modalities of the CS and respective contexts with the US. Because conditioning meets seven of eight implicit specifications it will be conceptualized here as being a component of the implicit-nondeclarative memory system (Squire, 1992). In summary, conditioning and other types of implicit learning and memory are learned out of awareness and are not later recallable or retrievable.

References

Badgaiyan, R.D., & Posner, M.I. (1997). Time course of cortical activations in implicit and explicit recall. Journal of Neuroscience, 17(12), 4904-13.

Bischoff-Grethe, A., Goedert, K.M., Willingham, D.T., & Grafton, S.T. (2004). Neural substrates of response-based sequence learning using fMRI. Journal of Cognitive Neuroscience, 16(1), 127-138.

Eichenbaum, H. (2002). The cognitive neuroscience of memory. New York: Oxford University Press.

Erdelyi, M.H. (1985). Psychoanalysis: Freud’s cognitive psychology. New York: WH Freeman & Co. (Chapter 2).

Garcia, R. (2002). Post-extinction of conditioned fear: between two CS-related memories. Learning and Memory, 9(6) 361-3.

Hamann, S.B., & Squire, L.R. (1997) Intact perceptual memory in the absence of conscious memory. Behavioral Neuroscience, 111(4), 850-4.

James TW, Humphrey GK, Gati JS, Menon RS, Goodale MA (2000). The effects of visual object priming on brain activation before and after recognition. Current Biology, 10(17), 1017-24.

Milner, B. (1972). Disorders of learning and memory after temporal lobe lesions in man. Clinical Neurosurgery, 19, 421-446.

Milner, B., Corkin, S., & Teuber, H.L. (1968). Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. Neuropsychologia, 6, 215-234.

Pavlov, I.P. (1927). Conditioned Reflexes. (Translated by G.V. Anrep) Cambridge: Oxford University Press (Lectures 2, 4, & 5).

Peinado-Manzano, A. (1988). Effects of bilateral lesions of the central and lateral amygdala on free operant successive discrimination. Behavioural Brain Research, 29(1-2), 61-71.

Peigneux, P., Maquet, P., Meulemans, T., Destrebecqz, A., Laureys, S., Degueldre, C., Delfiore, G., Aeerts, J., Luxen, A., Franck, G., Van der Linden, M., & Cleeremans, A. (2000). Striatum forever, despite sequence learning variability: a random effect analysis of PET data. Human Brain Mapping, 10(4), 179-94.

Pigott, S., & Milner, B. (1993). Memory for different aspects of complex visual scenes after unilateral temporal- or frontal lobe resection. Neuropsychologia, 31(1), 1-15.

Rauch, S.L., Walen, P.J., Curran, T., McInerney, S., Heckers, S., & Savage, C.R. (1998). Thalamic deactivation during early implicit sequence learning: a functional MRI study. Neuroreport, 9(5), 865-876.

Rauch, S.L., Whalen, P.J., Savage, C.R., Curran, T., Kendrick, A., Brown, H.D., Bush, G., Breiter, H.C., & Rosen, B.R. (1997). Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Human Brain Mapping, 5(2), 124-132.

Reber, P.J., Gitelman, D.R., Parrish, T.B., & Mesulam, M.M. (2003). Dissociating explicit and implicit category knowledge with fMRI. Journal of Cognitive Neuroscience, 15(4), 574-583.

Roediger, H.L. (1990). Implicit memory. Retention without remembering. American Psychologist, 45(9), 1043-1056.

Runyan, J.D., Moore, A.N., & Dash, P.K. (2004). A role for prefrontal cortex in memory storage for trace fear conditioning. Journal of Neuroscience, 24(6), 1288-1295.

Ryan, J.D., & Cohen, N.J. (2003). Evaluating the neuropsychological dissociation evidence for multiple memory systems. Cognitive, Affective, and Behavioral Neuroscience, 3(3), 168-185.

Schacter, D.L. (1987). Implicit memory: history and current status. Journal of Experimental Psychology, Learning, Memory and Cognition, 13(3), 501-518. Schacter, D.L. (1990). Perceptual representation systems and implicit memory. Toward a resolution of the multiple memory systems debate. Annals New York Academy of Sciences, 608, 543-567.

Schacter, D.L. (1992). Implicit knowledge: new perspectives on unconscious processes. Proceedings of the National Academy of Sciences, U.S.A., 89(23), 1113-1117.

Schacter, D.L. (1994). Implicit knowledge: new perspectives on unconscious processes. International Review of Neurobiology. 37, 271-84.

Schacter, D.L., Alpert, N.M., Savage, C.R., Rauch, S.L., & Albert, M.S. (1996). Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. Proceedings of the National Academy of Sciences U.S.A., 93(1), 321-325.

Schott, B.H., Henson, R.N., Richardson-Klavehn, A., Becker, C., Thoma, V., Heinze, H.J., & Duzel, E. (2005). Redefining implicit and explicit memory: The functional neuroanatomy of priming, remembering, and control of retrieval. Proceedings National Academy of Sciences U.S.A., 102(4), 1257-1262.

Squire, L.R. (1992). Memory and the hippocampus: a synthesis from findings with monkeys and humans. Psychological Reviews, 99(2), 195-231.

Squire, L.R. (2004). Memory systems of the brain: a brief history and current perspective. Neurobiology of Learning and Memory, 82(3), 171-177.

Squire, L.R., Knowlton, B., & Musen, G. (1993). The structure and organization of memory. Annual Review of Psychology, 44, 453-95.

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.

Willingham, D.B., Salidis, J., Gabrieli, J.D. (2002). Direct comparison of neural systems mediating conscious and unconscious skill learning. Journal of Neurophysiology, 88(3), 1451-1460.

Explicit-Declarative Memory

Explicit or declarative memory is memory that is derived from conscious awareness (Schacter, 1987). It is dependent on the relational processing capabilities of an intact hippocampus (Squire, 1992). As such it facilitates the ability for understanding the relationships between coactivated stimuli (S,S*) or events (White & McDonald, 2002). According to Larry Squire (1992) explicit or declarative memory is described as being accessible and as supporting cue/stimulus dependent and independent recognition and recall. It is fast learning; with developmental maturity, it can support quick one-trial learning. Though this type of memory’s learning has representational flexibility, it is also fallible. It is not associated with one specific sensory modality or context and not inextricably tied to the original learning context (Ryan & Cohen, 2003). Explicit and declarative learning involves complex multimodal associations (Squire et al., 1993). Finally its thought process is purposeful and intentional. In summary explicit or declarative memory is dependent on an intact hippocampus and is characterized by its capacity for recallable recognition and retrieval as well as stimulus-stimulus relational processing.

There are two forms of declarative memory, namely semantic and episodic (Squire, 1992). Semantic memory is memory for general facts and knowledge, e.g. names, places, dates, events, etc. One doesn’t remember exactly when, where, and how a certain fact is learned, only its byproduct is remembered and encapsulated in memory for the fact. Episodic memory (Tulving, 1983) begins with experiencing an event and ends with its subjective remembering or retrievable recall for the event. Its “mental reliving” involves the receipt, storage and retrievable recognition and recall of temporally linked and dated event-related information. Autobiographical memory is a type of episodic memory that is embedded with personal relevance. Episodic memory can be differentiated from semantic memory’s general knowledge by its self-referential uniqueness in time and space. Both are easily retrievable, fallible, fast learning, and in full awareness.

References

Ryan, J.D., & Cohen, N.J. (2003). Evaluating the neuropsychological dissociation evidence for multiple memory systems. Cognitive, Affective, and Behavioral Neuroscience, 3(3), 168-185.

Squire, L.R. (1992). Memory and the hippocampus: a synthesis from findings with monkeys and humans. Psychological Reviews, 99(2), 195-231.

Schacter, D.L. (1992). Implicit knowledge: new perspectives on unconscious processes. Proceedings of the National Academy of Sciences, U.S.A., 89(23), 11113-7.

Squire, L.R., Knowlton, B., & Musen, G. (1993). The structure and organization of memory. Annual Review of Psychology, 44, 453-95.

Tulving, E. (1983). Elements of episodic memory. New York: Oxford University Press (Chapter 9).

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.