Memory Systems

Before discussing childhood cognitive development, a brief discussion of memory and review of the animal and human research will help to contrast the different types of memory from one another. Memory is not a single entity. It is characterized by many different multiple parallel systems and neural circuits that occasionally interact in convergence zones in discrete regions of the brain, like the thalamus, hippocampal formation, striatum, cingulate cortex, etc. (Damasio, 1992). There is one type of memory called explicit-declarative memory. It supports conscious thought that underlies intentional behavior. It is accessible behaviorally and verbally due to its ability for recall and supports cue/stimulus dependent and independent recognition and recall. It is also fast-learning, flexible, associated with many different sensory modalities with complex multimodal associations, can be generalized across different learning environments, and is mediated by the structural integrity of the hippocampus and surrounding medial temporal lobe structures (Ryan & Cohen, 2003; Squire, 1992; Squire, Knowlton, & Musen, 1993). All these components are important for the development and for the later retrieval of personally meaningful autobiographical event memory.

There is another type of memory called implicit-nondeclarative memory. It is evidenced in nonconscious abilities as in perceptual priming skills, i.e. the ability for matching task-dependent sensory fragments to an image in its presence, and in learning procedural habits or motor sequences and skills. Its learning is characterized as inaccessible, due to its inability for deliberate recall  in the absence of a stimulus.  It is also modality-specific and harbors sensory data driven and behaviorally inferred qualities. It requires many repetitive learning trials to meet learning performance demands. It is also evidenced during early acquisition learning of emotional conditioning (Roediger, 1990; Schacter, 1990; Squire, 1992; Squire et al., 1993).

When critical components of a specific memory system or specific neural circuitry associated with either memory system are removed or destroyed, later task-related memory is impaired. For instance, when the explicit memory-associated fornix of the hippocampal region is removed in the rodent, deficits in informational processing about changing relationships among environmental cues for resolving feature ambiguity in spatial location have been noted as well as the slowing of learning acquisition (McDonald, Murphy, Guarraci, Gortler, While, & Baker, 1997; McDonald & White, 1995). To compensate for this region’s loss and the animal’s inability for recalling previously learned environmental features, the animal relies on implicit memory associated exteroceptive input from the sensory cortex to learn about immediate nonretrievable perceptual features (Badgaiyan & Posner, 1997) and the dorsal striatal-caudate motor system’s self-generated movements to gain egocentric information about the environment (Kesner, Bolland, & Dakis, 1993). On the other hand, neural inactivation of the implicit memory-associated dorsal striatal region allows for expression of hippocampal-mediated explicit memory processes of place learning as well as the uncontrollable and disruptive tendency for unintentionally retrieving previously learned behavioral sequences in new environments (DeCoteau & Kessner, 2000; Packard & McGaugh, 1996), suggesting that this region (dorsal striatum) is needed for the expression of new behavioral sequences. Another neural circuit that is characterized by implicit memory and emotional conditioning involves the amygdala-ventral striatum. This circuitry plays a crucial role in identifying anticipated cues that are associated with rewarding or aversive outcomes and reward mediating approach or avoidance behaviors respectively needed for facilitating emotional conditioning and learning (Chai & White, 2004; Holahan & White, 2002).

Human lesioning of the medial temporal lobe, including the hippocampal region, suggests that it is critically involved in the later ability for verbally declaring that which had been experienced and learned. For instance both a woman with Korsakoff’s syndrome and amnesics incurring destruction to the diencephalon (involving the thalamus) and medial temporal lobe (involving the amygdala &/ hippocampal region) respectively, were able to acquire early pain and classical eye-blink conditioning (Claparede, 1995; Weiskrantz & Warrington, 1979); however, when asked, they were unable to remember and describe their previous conditioning experiences despite verbal reminders. In fact, a circumscribed lesion of the hippocampus has the capacity for impairing the ability for acquiring and verbally reporting declarative facts about task-related stimulus-context relationships but has no effect on the acquisition of a conditioned autonomic response (Bechara, Tranel, Damasio, Adolphs, Rockland, & Damasio, 1995). A lesion of the amygdala impaired a patient’s acquisition of conditioned autonomic responses of increased skin conductance (Glascher & Adolphs, 2003) to a startling sound but spared the ability for acquiring and verbally reporting task-related declarative facts about task-related stimulus-context relationships (Bechara,et al. 1995).  These findings suggest that the amygdala processes material via its interaction with structures tied with autonomic activity; the hippocampus is involved in the ability for gaining and reporting declarative knowledge about stimulus-context relationships. 

According to the above-noted lesioning research each memory system interacts with one another, has a temporally determined contribution, and, in its absence, allows for the expression of other memory systems to meet task dependent demands (Poldrack & Rodriguez, 2004; White & McDonald, 2002). The lesioning research also suggests that any compensatory response by expressed regions will be wholey limited by their inherent regional functional specialization.

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.

Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., & Damasio, A.R. (1995). Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science, 269(5227), 1115-8.

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.

Claparede, E. (1911). Recognition and selfhood (Subsequently translated by Anne-Marie Bonnel & published in 1995). Consciousness and Cognition, 4(4), 371-8. Damasio, A.R. (1989). The brain binds entities and events by multiregional activation from convergence zones. Neural Computing, 1, 123-32.

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.

Glascher, J., & Adolphs, R. (2003). Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala. Journal of Neuroscience, 23(32), 10274-82.

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. (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.

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

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. (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.

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., Knowlton, B., & Musen, G. (1993). The structure and organization of memory. Annual Review of Psychology, 44, 453-95. Weiskrantz, L., & Warrington, E.K. (1979). Conditioning in amnesic patients. Neuropsychologia, 17, 187-194.

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.

Memory Development

Memory is manifested in neural networks throughout the brain that intersect in specific regions like the thalamus, striatum, hippocampus, dorsolateral prefrontal cortex, cingulate cortex, etc. Early theories hypothesized that subcortical implicit memory was the predominant form of learning during first year. Today however researchers believe the brain develops contemporaneously.

Both implicit and explicit processes develop at the same time soon after birth onward. For many years, based on the findings of developmental nonhuman primate research, it was assumed that the earliest of preverbal infants’ behavioral learning was reflective of implicit perceptual motor learning and memory expression. However, recent delayed recognition tests suggest otherwise. Research that monitors intrinsically reinforcing motor learning after one day of training suggests that a three month old infants’ abilities at learning to intentionally kick a crib mobile during one single fifteen minute session and the ability for cue dependent and independent recall is reflective of explicit rather than implicit processes (for a review, see Rovee-Collier, 1997). Furthermore these training sessions were contextually dependent, i.e. infants did not generalize learned kicking behavior to a new mobile in a new crib setting (Rovee-Collier, 1990). Findings that three month old infants can remember previously learned context-dependent tasks coupled with those reflecting respective object size sensitivity and insensitivity in total, suggest that both explicit and implicit learning and their respective “memory systems develop in parallel rather than hierarchically during the first year of life” (Gerhardstein, Adler, & Rovee-Collier, 2000, p. 132).

Moreover Yakolev & Lecours (1967) research findings on ontogenetic myelin development suggested a hierarchal temporally sequenced developmental pattern for CNS and brain development, with the magnitude of prenatal and earliest of postnatal neuronal growth initiating in the spinal column, brain stem, and subcortical structures and then later spreading to neocortical regions. According to Patricia Goldman-Rakic and colleagues these findings contrast with findings in the nonhuman primate, which suggest a concurrent and concomitant manner (Goldman-Rakic, Bourgeois, & Rakic, 1997). They also challenged the hierarchal growth pattern hypothesis in response to stark ambiguities and exceptions. They cited that the corticospinal motor system is among the last brain regions to myelinate. They also noted that the sensory association area never really fully myelinates like other brain regions (including the prefrontal cortex, which is presumed to be one of the last brain region to myelinate). Furthermore the corpus callosal axons connecting to sensory association areas myelinate a good deal less than those in the sensory association areas. In response to these discrepancies Goldman-Rakic and colleagues have concluded that human primate brain development likely matches the pattern of the nonhuman primate. According to their analysis of the research in the nonhuman primate, postnatal synaptogenesis and neurogenesis, occurs “contemporaneously” in many different neocortical regions (Rakic, Bougeois, Eckenhoff, et al., 1986). However, there seems to be a timetable for neurotransmitter receptor expression, i.e. for dopamine, serotonin, and noradrenaline receptors in different laminae throughout the whole brain (Lidow, Goldman-Rakic, & Rakic, 1991). Moreover cells in laminae VI and V in the visual cortex develop earlier than neurons in layers II and I, which project through the corpus callosum or by commissures (Trevarthen, 1986). These findings are supported by a cross-sectional positron emission tomography (P.E.T.) study that measured local cerebral glucose metabolism (lCMRGlc) rates (Chugani, Phelps, & Mazziotta, 1987). The reported data demonstrated annualized interregional glucose utilization patterns with striking similarities. Cerebral glucose utilization patterns stabilized at ranges of 17.59-27.15 levels during the first year, 19.50-32.39 levels in the second year, and 30.74-61.01 levels in the third year, etc. However daily (and probably weekly and monthly) variability was noted to likely exist. This was supported by the authors’ referencing one five day old subject, who demonstrated greater glucose utilization in the thalamus and basal ganglia when compared with other brain regions. The annualized data though showed similar regional activity throughout the brain. The existing research seems to suggest a “contemporaneous” brain developmental pattern but local growth variability (probably relating to local neurotransmitter expression) the laminae in discrete regions of the brain at any point in time.

Within this whole brain growth construct a within region analysis demonstrated some variability in overall growth rates in the whole brain (Rabinowicz, 1986). For instance in the human the ages from 15-24 months are characterized by growth that allows all regions and layers to reach similar states of maturation. Another time period, 6-8 years, is characterized by remodeling of the cortex, i.e. its thickness, number of neurons and neuronal dendrites. Growth spurts in all regions, possibly evidence of remodeling, also seem to occur between 10-12 years and finally at 18 years. As noted in subsequent sections these growth spurts may be reflective of neural growth supporting aspects relating to developmental milestones relating to sense of self and theory of mind. Again brain growth is likely characterized by “contemporaneous” growth, with variations in growth in certain laminae or in whole brain growth at certain key ages.

References

Chugani, H.T., Phelps, M.E., & Mazziotta, J.C. (1987) Positron emission tomographic study of human brain functional development. Annals of Neurology, 22, 487-497.

Gerhardstein, P., Adler, S.A., & Rovee-Collier, C. (2000). A dissociation in infants’ memory for stimulus size: evidence for the early development of multiple memory systems. Developmental Psychobiology, 36(2), 123-135.

Goldman-Rakic, P.S., Bourgeois, J.P., & Rakic, P. (1997). Synaptic stustrate of cognitive development life-span analysis of synaptogenesis in the prefrontal cortex of the nonhuman primate. In: N.A. Krasnegor, G.R. Lyon, P.S. Goldman-Rakic (Eds.) Development of the prefrontal cortex, (pp. 27-47), Baltimore, MD: Brookes.

Lidow, M.S., Goldman-Rakic, P.S., Rakic, P. (1991). Synchronized overproduction of neurotransmitter receptors in diverse regions of the primate cerebral cortex. Proceedings of National Academy of Sciences, U.S.A., 88, 10218-10221.

Rabinowicz, T. (1986). The differentiated maturation of the cerebral cortex. In: F. Falkner, & Tanner, J.M. (Eds.) Human Growth, (pp. 385-410), New York: Plenum Press.

Rakic, P., Bourgeois, J.P., Eckenhoff, M.F., Zecevic, N., Goldman-Rakic (1986). Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science, 232, 232-235.

Rovee-Collier, C. (1990). The “memory system” of prelinguistic infants. Annals of New York Academy of Sciences, 608, 517-536.

Rovee-Collier, C. (1997). Dissociations in infant memory: rethinking the development of implicit and explicit memory. Psychological Review, 104(3), 467-498.

Trevarthen, C.B. (1986). Neuroembryology and the development of perceptual mechanisms. In: In: F. Falkner, & Tanner, J.M. (Eds.) Human Growth, (pp. 301-383), New York: Plenum Press.

Yakovlev, P.I., & LeCours, A.R. (1967). The myelogenetic cycles of regional maturation of the brain. In: A. Minkowsky (Ed.), Regional development of the brain in early life (pp. 3-70). Oxford, UK: Blackwell Scientific.