Memory in the Cortex of the Primate

Biol Res 28: 59-72 (1995) 59 Memory in the cortex of the primate JOAQUIN M FUSTER Department of Psychiatry, School of Medicine, University of California at Los Angeles, Los Angeles, CA, USA Memory is viewed as hierarchical and distributed in primary and association areas of cerebral cortex. Different memory neural networks are interconnected at various levels in this hierarchy, sharing neurons and connections. All memory is essentially associative in its generation, structure and retrieval. External and internal stimuli, to which we attend by virtue of their biological relevance or for other reason, can at any time activate ("turn on ") the neuronal network to which they belong by previous association. This is the basis of knowledge and remembering. The reverberation in recurrent circuits may keep the network in an active state, that is, serving behavior, attention and consciousness. Monkey neuropsychological and electrophysiological data, and human tomographic (brain metabolism) evidence are presented supporting these concepts. Key terms: association cortex, associative memory, prefrontal cortex. INTRODUCTION GENERAL PRINCIPLES In the first place, I will try to present an I will start by stating some general principles overall vision of the role of the cerebral of memory that derive from neuropsycho cortex in memory, a vision which, although logical and neurophysiological work in the somewhat personal and perhaps too am last years. Some of these principles are still bitious, harmonizes with the evidence that in an embryonic stage, reason for which we through many years we have been accu cannot blindly accept them. However, for the mulating in my laboratory. In second place, I sake of brevity, they can be accepted at least will try to suggest a working plan, an agenda as working hypotheses and as premises for for future research, a guide to shed some the experiments that I shall try to summarize light on the still obscure but fascinating and below: complex subject of memory. More precisely, here it will be discussed 1. Memory is a widely distributed func (1) how cortical memory is formed; (2) tion. All neural systems have memory. Each where it is formed; and (3) how it is ac component of the central nervous system, tivated. In relation to the third point, particu each system or subsystem of the brain has its lar attention will be given to one aspect of memory, memory whose contents strictly cortical dynamics about which we have some depends on the information processed by it; experience in our laboratory. It concerns thus, there is sensory memory in sensory the dynamic structure of associative net systems, visual memory, auditory memory, works and their activation during recognition haptic memory, etc, ... motor memory in mo as well as in the temporal retention of mem tor systems, visceral memory in visceral con ory. trol systems, etc. In each of these systems, Correspondence to: Joaquin M Fuster. Department of Psychiatry. UCLA School of Medicine. 760 Westwood Plaza, Los Angeles, CA 90024-1759. USA. Fax: (1-310) 825-6792 60 Biol Res 28: 59-72 (1995) memory forms an integral part in the pro formed by association, is maintained by as cessing of the information in which the sys sociation, and is evoked, remembered, by tem specializes; in fact, representation and association. processing share the same neuronal networks 4. The structure and contents of cortical within each system. Therefore, in neurophys- memory are hierarchically organized, as cor iological terms it does not make much sense responds to the organization of the informa to speak of systems of memory, but it does tion processing systems constituting these make sense to speak of memory of systems. networks. This hierarchical organization is This is a Copernican turn that I believe is adjusted, at least in a crude manner, to the worth making in our way of thinking if we phylogenetic and ontogenetic order that, as intend to get to some understanding of the we know, is a hierarchical development. To neurobiological basis of memory. understand this better, it is worth observing 2. Systems that interest us are cortical the ontogenetic map of human cortex. systems, and therefore we will be speaking Figure 1 presents the ontogenetic map of the memory of the cerebral cortex, as according to Flechsig (1901) and Von Bonin cortical memory. This fits everything, that is, (1950). Numbers do not indicate here dif all classes of memory that are investigated in ferent architectonic areas, but the order in modern neuropsychology. In the perceptual which the different cortical areas become sectors of associative cortex, at different myelinated, that is, the order in which their levels in its hierarchy, we find from down to extrinsic and intrinsic fibers develop their top unimodal sensory memory, multimodal myelin sheaths. Somehow there is a certain sensory memory, episodic memory, semantic correlation between myelinization and the memory and conceptual memory. Cortical other indexes of ontogenetic maturation memory is therefore the basis of what we call around and after birth, and the map thus cognitive memory, the base of knowledge approximately reflects the maturation of and personal experience. On the other hand, neocortical systems and the functionally in the associative sectors of the frontal lobe, hierarchical development of these systems. we find the plans, action schemes and pro This development and its hierarchy them grams in all aspects of motility (skeletal, selves result from the -also hierarchical- phy ocular, phonetic, etc), from the more abstract logenetic evolution of the cortex. to the more concrete, all plans and programs Thus, at the lowest level of cortical hier constituting what we call motor memory. archy, I find the primary sensory and motor Moreover, there in the frontal lobe, we find areas, here in black and with the lowest the mechanisms of organization of the ac numbers (Fig 1). These are presumably the tions in the temporal domain in order to first ones to develop. Soon after birth, the implement those plans and motor programs. organization and connectivity of these areas 3. A cortical memory, of any kind, the is complete, and their functions are prac "engram", so to speak, is a more or less ex tically identical to those of the adult organ tended neuronal network of interconnected ism, although it is also true that before they neurons. Depending on its complexity and its must undergo some critical postnatal periods conceptual or semantic contents, this net of functional exercise. These areas could be work may be circumscribed to a specific considered as the anatomical basis of what I cortical area or can be extended to different call phyletic memory, or species memory areas with association tentacles of varying (Fuster, 1994). This would be a form of ele length and convolutedness. Some of these mentary memory, common to all the association tentacles cross from one hemi members of a species, that has developed sphere to the other through the corpus callo- through innumerable generations and by the sum. Thus, in its neurobiological aspect, all same mechanisms of temporal coincidence as memory is a fundamentally associative struc those involved in the generation of individual ture, defined by the neuronal assemblies memory, of which we will speak below. The constituting it and by their connections. term "phyletic memory", although seeming a Similarly, in its psychological aspect, all little esoteric and arbitrary, does not need to memory is an associative phenomenon. It is alarm anyone, since I use it to characterize Biol Res 28: 59-72 (1995) 61 Fig 1. Myelogenetic map of the human cortex. something that is perfectly well established. urally idiosyncratic information that the indi It is nothing more than a different term for vidual accumulates along its life. Some the sensory and motor devices we are born caveats are necessary before going on: with. Thus, the neuronal networks of primary 1. What I just said does not imply that the cortex, with their proverbial modules and structure of primary areas comes to us al columns, would constitute the basis of the ready specified and unchangeable at birth. In mnemonic cortical hierarchy, predisposed to the first place, there are critical periods in "re-cognize" what the species already knows, their development, to which I have alluded, that is, the most elementary sensory and mo where use is necessary for the definitive func tor attributes. Beyond and over those primary tional maturation of these areas. These would areas in the connective and developmental be like training periods of phyletic memory, trajectory, are the areas labeled in gray (Fig needed by the organism in order to freely 1), and then in white, constituting the asso practice it. In second place, it has been well ciation cortex and conforming the personal demonstrated that these primary areas retain memory networks. These networks are form their plasticity even in the adult, a fact that ed there to represent and process the nat is apparent in the spontaneous or induced 62 Biol Res 28: 59-72 (1995) rehabilitation of their functions after certain post-rolandic cortex, with its large associa lesions (Merzenich and Kaas, 1982). tive region, is involved not only in the pro 2. This does not mean either that the cessing of perception but in perceptual mem substrate of associative memory comes to ory, including all those memory forms that the world to be made. On the contrary, all its are acquired by the senses (declarative, ep cytoarchitectonic and neurochemical struc isodic, semantic, etc). Pre-rolandic cortex, on ture seems already genetically determined, at the other hand, is mainly involved in the pro least in the monkey. What probably remains cessing and representation of action (includ to be done is the synaptic infrastructure at the ing the so-called "procedural memory"). finer levels, that is, the proteic basis deter The cytoarchitectonic map of Figure 2 mining the variability and facility of trans (Brodmann) shows the two components, mission of preexisting synapses.

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