Explicit (Declarative) Memory & the MTL

Explicit and declarative memory needs the support of and is dependent on a functional medial temporal lobe MTL (Squire, 1992). Loss of hippocampal viability causes deficits in retrievable recognition and in recollection of human faces, identification of voices, spoken words, and in acquiring definitions. Its loss also impairs the acquisition of allocentric information, i.e. acquiring associational relationships between objects with their locations and words in their temporal positions (Mayes, Holdstock, Isaac, Montaldi, Grigor, Gummer et al., 2004; Yonelinas, Kroll, Quamme, Lazzara, Sauve, Widaman et al., 2002). Destruction to the hippocampal system impairs delayed recall, recognition ability, declarative knowledge and awareness of repeating sequences (Squire, Schmolck, & Stark, 2001; Stefanacci, Buffalo, Schmolck, & Squire, 2000). Patients with amnesia syndrome and damage to the MTL have spared implicit-nondeclarative memory but lose their ability for spontaneous recall of recently learned facts or interpersonal experiences as noted in the patient, H.M., earlier.

Neuroimaging findings also support the essential role of the hippocampal region in facilitating semantic processing (Heckers, Weiss, Alpert, & Schacter, 2002; Wagner, Schacter, Rotte, Koutstaal, Maril, Dale et al., 1998) and intentional learning (Reber, Gitelman, Parrish, & Mesulam, 2003). Regional cerebral blood flow (rCBF) activations in the left mid-anterior hippocampus along with the parahippocampal gyrus, amygdala and medial prefrontal cortex facilitate the retrieval of recent and personally meaningful autobiographical memory (Maguire & Frith, 2003; Maguire & Mummery, 1999; Piefke, Weiss, Zilles, Markowitsch, & Fink, 2003). The anterior hippocampus with the amygdala facilitates the retrieval of personally relevant emotional episodes (Maguire & Frith, 2003) involving emotions of happiness, anger, or fear in interaction with cortical regions (Damasio, Grabowski, Bechara, Damasio, Ponto, Parvizi, & Hichwa, 2000) like the medial (Vogt, Berger, & Derbyshire, 2003) and anterior (Macrae, Moran, Heatherton, Banfield, & Kelley, 2004) prefrontal cortices. The hippocampus in coordination with other brain regions facilitates explicit episodic autobiographical memory.

The hippocampus also has a role in mediating the retrieval of conjunctive information of episodic memory. It binds a variety of sensory, affective, cognitive and behavioral elements of experiences associated with an event into a cohesive episode (Davachi, 2004; Jackson & Schacter, 2004). The hippocampal region, as such binds object, temporal, and contextual information to create a retrievable coherent and sequential internal representation of an episode’s what, where, and when (Ergorul & Eichenbaum, 2004; Fortin, Agster, & Eichnbaum, 2002). Organizing neural information in this way enhances retrieval of long term memory’s formation, storage, and retrieval.

The ability for performing relational memory processing about the nature of relationships between items also depends critically on an intact hippocampus. The hippocampus mediates the comparisons and relations between different individual representations with one another along with their relationship with coexisting memory structures and organization. As novel items and new information are encountered, the hippocampus processes how they relate to personally meaningful and existing schema (Eichenbaum & Cohen, 2001). Hippocampal activity and relational processing also correlates with the enhanced ability for later successful retrieval (Davachi & Wagner, 2002). It is through this capability that the hippocampus mediates flexible declarative (explicit) learning and retrievable memory. It makes “a unique contribution that allows lessons from the past to be applied to the future” (Preston, Shrager, Dudukovic, & Gabrieli, 2004, p. 150). Successfully completed psychotherapy noted later on may also mediate these processes as well.

References

Damasio, A.R., Grabowski, T.J., Bechara, A., Damasio, H., Ponto, L.L., Parvizi, J., & Hichwa, R.D. (2000). Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neuroscience, 3(10), 104-56.

Davachi, L. (2004). The ensemble that plays together, stays together. Hippocampus, 14(1), 1-3.

Davachi, L., & Wagner, A.D. (2002). Hippocampal contributions to episodic encoding: insights from relational and item-based learning. Journal of Neurophysiology, 88(2), 982-990.

Eichenbaum, H., & Cohen, N.J. (2001). From conditioning to conscious recollection. New York: Oxford University Press.

Ergorul, C., & Eichenbaum, H. (2004). The hippocampus and memory for “What,” “Where,” and “When.” Learning & Memory, 11, 397-405.

Fortin, N.J., Agster, K.L., & Eichnbaum, H.B. (2002). Critical role of the hippocampus in memory for sequences of events. Nature Neuroscience, 5(5), 458-62.

Heckers, S., Weiss, A.P., Alpert, N.M., & Schacter, D.L. (2002). Hippocampal and brain stem activation during word retrieval after repeated and semantic encoding. Cerebral Cortex, 12(9), 900-907.

Jackson, O. 3rd , & Schacter, D.L. (2004). Encoding activity in anterior medial temporal lobe supports subsequent associative recognition. Neuroimage, 21(1), 456-462.

Macrae, C.N., Moran, J.M., Heatherton, T.F., Banfield, J.F., & Kelley, W.M. (2004). Medial prefrontal activity predicts memory for self. Cerebral Cortex, 14(6), 647-654.

Maguire, E.A., & Frith, C.D. (2003). Lateral symmetry in the hippocampal response to the remoteness of autobiographical memories. Journal of Neuroscience, 23(12), 5302-7.

Maguire, E.A., & Mummery, C.J. (1999). Differential modulation of a common memory retrieval network revealed by positron emission tomography. Hippocampus, 9(1), 54-61.

Mayes, A.R., Holdstock, J.S., Isaac, C.L., Montaldi, D., Grigor, J., Gummer, A., Cariga, P., Downes, J.J., Tsivilis, D., Gaffan, D., Qiyong, G, & Norman, K.A. (2004) Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition. Hippocampus, 14, 763-84.

Piefke, M., Weiss, P.H., Zilles, K., Markowitsch, H.J., & Fink, G.R. (2003). Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. Brain, 126(Pt 3), 650-68.

Preston, A.R., Shrager, Y., Dudukovic, N.M., & Gabrieli, J.D. (2004). Hippocampal contribution to the novel use of relational information in declarative memory. Hippocampus, 14(2), 148-52.

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), 574-83.

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., Schmolck, H., & Stark, S.M. (2001) Impaired auditory recognition memory in amnesic patients with medial temporal lobe lesions. Learning and Memory, 8(5), 252-6.

Stefanacci, L., Buffalo, E.A., Schmolck, H., & Squire, L.R. (2000) Profound amnesia after damage to the medial temporal lobe: a neuroanatomical and neuropsychological profile of patient E.P. Journal of Neuroscience, 20(18), 7024-36.

Vogt, B.A., Berger, G.R., & Derbyshire, S.W. (2003). Structural and functional dichotomy of human midcingulate cortex. European Journal of Neuroscience, 18(11), 3134-44.

Wagner, A.D., Schacter, D.L., Rotte, M., Koutstaal, W., Maril, A., Dale, A.M., Rosen, B.R., & Buckner, R.L. (1998). Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science, 281(5380), 1188-91.

Yonelinas, A.P., Kroll, N.E., Quamme, J.R., Lazzara, M.M., Sauve, M.J., Widaman, K.F, & Knight, R.T. (2002). Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nature Neuroscience, 5(11), 1236-41.

Implicit (Nondeclarative) Memory & the MTL

The hippocampal region (included in the medial temporal lobe (MTL) region) also enhances implicit cue-in-context and object-in-scene relations (Eichenbaum, 1999). It supports early perceptual learning by processing novel physical features of perceptual stimuli (Strange, Fletcher, Henson, Friston, & Dolan, 1999) and implicit sequence learning (Schendan, Searl, Melrose, & Stern, 2003). In motor sequence learning it later facilitates recognition of previously encountered sequences (Muller, Kleinhans, Pierce, Kemmotsu, & Courchesne, 2002). The hippocampal region supports implicit perceptual learning when learning conditions are compromised by temporal brevity (Degonda, Mondadori, Bosshardt, Schmidt, Boesiger, Nitsch, et al., 2005) and perceptual noise patterns (Henke, Treyer, Nagy, Kneifel, Dursteler, Nitsch, & Buck, 2003). Finally it facilitates the detection of the hidden rule underlying complex perceptual relational processing (Rose, Haider, Weiller, & Buchel, 2002, 2004).  Therefore the hippocampal region helps to support both implicit memory processing that is not in conscious awareness and explicit purposeful memory processing.

In summary, the hippocampal region plays a supportive role in implicit and nondeclarative learning and memory, by processing novelty information and enabling successful later recognition of perceptual information. It also supports learning when the conscious perception of stimuli is impaired and when increasing cognitive demands necessitate complex perceptual relational processing.

References

Degonda, N., Mondadori, C.R., Bosshardt, S., Schmidt, C.F., Boesiger, P., Nitsch, R.M., Hock, C., & Henke, K. (2005). Implicit associative learning engages the hippocampus and interacts with explicit associative learning. Neuron, 46(3), 505-520.

Eichenbaum, H. (1999). Conscious awareness, memory, and the hippocampus. Nature Neuroscience, 2(9), 775-776.

Henke, K., Treyer, V., Nagy, E.T., Kneifel, S., Dursteler, M., Nitsch, R.M., & Buck, A. (2003). Active hippocampus during nonconscious memories. Conscious Cognition, 12(1), 31-48.

Muller, R.A., Kleinhans, N., Pierce, K., Kemmotsu, N., & Courchesne, E. (2002). Functional MRI of motor sequence acquisition: effects of learning stage and performance. Brain Research Cognitive Brain Research, 14(2), 277-293.

Rose, M., Haider, H., Weiller, C., & Buchel, C. (2002). The role of medial temporal lobe structures in implicit learning: an event-related fMRI study. Neuron, 36(6), 1221-1231.

Rose, M., Haider, H., Weiller, C., & Buchel, C. (2004). The relevance of the nature of learned associations for the differentiation of human memory systems. Learning & Memory, 11(2), 145-152.

Schendan, H.E., Searl, M.M., Melrose, R.J., & Stern, C.E. (2003). An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron, 37(6), 1013-1025.

Strange, B.A., Fletcher, P.C., Henson, R.N., Friston, K.J., & Dolan, R.J. (1999). Segregating the functions of human hippocampus. Proceedings of National Academy of Sciences U.S.A., 96(7), 4034-4039.