Wendy A. Suzuki

The Organization of Memory in the Medial Temporal Lobe

Humans and animals have an amazing ability to learn and retain new information for facts and events. This form of memory is termed declarative memory in humans and relational memory in animals. Strong evidence has demonstrated that an interconnected set of brain structures in the medial temporal lobe including the hippocampus and surrounding entorhinal, perirhinal and parahippocampal cortices contribute critically to declarative/relational memory. It remains unclear, however, how the individual brain areas contribute to this form of memory. Do all areas contribute in a unitary way to declarative/relational memory, or is each structure specialized for certain forms of memory? What are the neural mechanisms underlying memory in these areas? How do these areas interact with extra-medial temporal lobe brain areas during the acquisition and retrieval processes?

The major goal the Suzuki Laboratory is to understand the neural signals underlying the formation and representation of declarative/relational memory in the monkey brain. One form of declarative/relational memory we have focused on is associative memory, defined as the ability to associate two unrelated items in memory. We have shown that many cells in the monkey hippocampus signal learning of new associations with dramatic changes in their firing rate (Wirth et al., 2003). Recent functional imaging studies have shown that similar changes in activity are seen in the human medial temporal (Law et al., 2005). We have also shown that hippocampal neurons signal well- learned information with a significantly more selective response compared to novel information (Yanike et al., 2004). Current work is examining how the hippocampus interacts with other brain areas during the associative learning process. Another major goal in the lab is the development of a novel battery of medial temporal lobe-dependent memory tasks to use in our neurophysiological studies. This battery includes tasks of temporal order memory designed to mimic the kind of memory required in episodic memories, a form of declarative/relational memory. We are also in the process of developing a novel family of naturalistic memory tasks based on memory for social interactions that are designed to tap the natural learning and memory tasks that monkeys have evolved to solve. A long-term goal is to understand not only how medial temporal lobe areas contribute to theses tasks, but also how the medial temporal lobe may interact with other brain areas including the prefrontal cortex and striatum during both acquisition and retrieval of declarative/relational information.

E-mail: wendy@cns.nyu.edu

Representative Publications

Zola-Morgan, S., Squire, L.R., Amaral, D.G., and Suzuki, W.A. (1989). Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J. Neurosci. 9, 4355-4370.

Suzuki, W.A., Amaral, D.G. (1990). Cortical inputs to the CA1 field of the monkey hippocampus originate from the perirhinal and parahippocampal cortex, but not from TE. Neurosci. Let. 115:43-48.

Suzuki, W.A., Zola-Morgan, S., Squire, L.R., and Amaral, D.G. (1993). Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J. Neurosci. 13, 2430-2451.

Suzuki, W.A. and Amaral, D.G. (1994). Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents. J. Comp. Neurol. 350, 497-533.

Suzuki, W.A. and Amaral, D.G. (1994). Topographic organization of the reciprocal connections between monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J. Neurosci. 14, 1856-1877.

Suzuki, W.A. (1996). The anatomy, physiology and functions of the perirhinal cortex. Cur. Opin. Neurobio. 6, 179-186.

Stefanacci, L., Suzuki, W.A., and Amaral, D.G. (1996). Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys. J. Comp. Neurol. 375, 552-582.

Mishkin, M., Suzuki, W.A., Gadian, D.G., and Vargha-Khadem, F. (1997). Hierarchical organization of cognitive memory. Philos. Trans. R. Soc. Lond.[ Biol]. 352, 1461-1467.

Suzuki, W.A., Miller, E.K., and Desimone, R. (1997). Object and place memory in the macaque entorhinal cortex. J. Neurophys. 78, 1062-1081.

Suzuki, W.A. (1999). The long and the short of it: Memory signals in the medial temporal lobe. Neuron 24, 295-298.

Suzuki, W.A. and Eichenbaum, H. (2000). The Neurophysiology of Memory. Annals of the New York Acad. Sci. 911, 175-191.

Suzuki, W.A. and Clayton, N.S. (2000). The hippocampus and memory: a comparative and ethological perspective. Cur. Opin. Neurobio. 10, 768-773.

Suzuki, W.A. and Porteros, A. (2002). Distribution of calbindin D-28k in the entorhinal, perirhinal and parahippocampal cortices of the macaque monkey. J. Comp. Neurol. 451, 392-412.

Lavenex, P., Suzuki, W.A., and Amaral, D.G. (2002). Perirhinal and parahippocampal cortices of the macaque monkey: projections to the neocortex. J. Comp. Neurol. 447, 394-420.

Wirth, S., Yanike, M., Frank, L.M., Smith, A.C., Brown, E.N., and Suzuki, W.A. (2003). Single neurons in the monkey hippocampus and learning of new associations. Science 300, 1578-1581.

Suzuki, W.A. (2003). Declarative versus episodic: Two theories put to the test. Neuron 37, 5-7.

Suzuki, W.A. and Amaral, D.G. (2003). Where are the perirhinal and parahippocampal cortices? A Historical overview of the nomenclature and boundaries applied to the primate medial temporal lobe. Neuroscience 120, 893-906.

Suzuki, W.A. and Amaral, D.G. (2003). The perirhinal and parahippocampal cortices of the macaque monkey: Cytoarchitectonic and chemoarchitectonic organization. J. Comp. Neurol. 463, 67-91.

Suzuki, W.A. and Amaral, D.G. (2004). Functional neuroanatomy of the medial temporal lobe memory system. Cortex 40, 220-222.

Yanike, M., Wirth, S., and Suzuki, W.A. (2004) Representation of well-learned information in the monkey hippocampus. Neuron 42, 477-487.

Buckmaster, C.A., Eichenbaum, H., Amaral, D.G., Suzuki, W.A., and Rapp, P.R. (2004) Entorhinal cortex lesions disrupt the relational organization of memory in monkeys. J. Neurosci. 24, 9811-9825.

Smith, A.C., Frank, L.M., Wirth, S., Yanike, M., Hu, D., Kubota, Y., Graybiel, A.M., Suzuki, W.A., and Brown, E.N. (2004) Dynamic analysis of learning in behavioral experiments. J. Neurosci. 24, 447-461.

Lavenex, P., Suzuki, W.A., and Amaral, D.G. (2004) Intrinsic perirhinal and parahippocampal cortices of the macaque monkey: Intrinsic projections and interconnections. J. Comp. Neurol. 472, 371-394.

Suzuki, W.A. and Brown, E.N. (2005). Behavioral and neurophysiological analysis of dynamic learning processes. Behavioral and Cognitive Neurosci. Rev. 4. 67-95.

Law JR, Flanery MA, Wirth S, Yanike M, Smith AC, Frank LM, Suzuki WA, Brown EN and Stark CEL (2005) fMRI activity during the gradual acquisition and expression of paired associate memory. J Neurosci 25, 5720-5729.

Byrne JH and Suzuki WA (2006) Neurbiology of behavior. Editorial overview. Curr. Opin Neruobio. 16:6680:671.

Suzuki, W.A. (2006). Encoding new episodes and making them stick. Neuron 50, 19-21.

Smith AC, Wirth S, Suzuki WA and Brown EN (2007) Baysian Analysis of interleaved learning and response bias in behavioral experiments. J. Neurophys. 97, 2516-2524.

Suzuki WA (2007) Integrating associative learning signals across the brain. Hippocampus. 17:842-50.

Suzuki WA (2007) Making new memories: The role of the hippocampus in new associative learning. In: Imaging and the aging brain. Eds. deLeon MJ, Snider DA, Federoff H. Ann. NY Acad. Sci. 1097:1-11.

Suzuki WA (2007) Making and retaining new memories: The role of the hippocampus in associative learning and memory. In: Memories: Molecules and Circuits. Eds. Bontempi, B Silva AJ and Cristen Y. Springer-Verlag Berlin. pp 113-124.

Suzuki WA (2008) Declarative memory systems: Anatomy. In: Encyclopedia of Neurosceince Volume 3. Ed. Squire LR. Oxford: Academic Press. Pp 347-356.

Czanner G, Eden UT, Wirth S, Yanike M, Suzuki WA, and Brown EN (2008) Analysis of between-and within-trial neural spiking dynamics. J. Neurophys. 99, 2672-2693.

Prerau MJ, Smith AC Eden UT, Yanike M, Suzuki WA and Brown EN (2008) A mixed filter algorithm for cognitive state estimation from simultaneously recorded continuous and binary measures of performance. Biol. Cyberntics 99:1-14.

Wirth S, Avsar E, Chiu CC, Sharma V, Smith AC, Brown EN, Suzuki WA (2009) Trial outcome and associative learning signals in the monkey hippocampus. Neuron 61, 93-940.

Yanike M, Wirth S, Smith AC, Brown EN, Suzuki WA (2009) Comparison of associative learning-related signals in the macaque perirhinal cortex and hippocampus. Cerebral Cortex 19, 1064-1078.

Prerau MJ, Smith AC Eden UT, Kubota Y, Yanike M, Suzuki W, Graybiel AM and Brown EN (2009) Characterizing learning by simultaneous anlaysis of continuous and binary measures of performance. J. Neurophys. In press.

Suzuki, WA (2009) Perception and the medial temporal lobe: Evaluating the current evidence. Neuron. 61, 657-666.

Suzuki WA and Baxter MG (2009) Memory, perception and the medial temporal lobe: A synthesis of opinions. Neuron. 61, 678-679.

Suzuki WA (2009) Comparative Analysis of the cortical afferents, intrinsic projections and interconnections of the parahippocampal region in monkeys and rats. In: The Cognitive Neurosciences. Ed. Gazzaniga MS. In press (Coming soon).