Principles of Memory Organization in the Monkey Medial Temporal Lobe Wendy A. Suzuki Center for Neural Science New York University

24/25/32 Pi Ia Id Ig Frontal LobeTemporal LobeInsular Cortex Cingulate Gyrus Parietal Lobe V4 23/29/30 7a/LIP STSdSTG TE STSv TEO 11/ DG Sub HPC 30-60% 18-29% 5-17% <5% Entorhinal Parahippocampal Perirhinal Suzuki and Amaral, 1994

Take Home Message: All structures of the MTL appear to provide a similar complement of associative learning- related signals.

24/25/32 Pi Ia Id Ig Frontal LobeTemporal LobeInsular Cortex Cingulate Gyrus Parietal Lobe V4 23/29/30 7a/LIP STSdSTG TE STSv TEO 11/ DG Sub HPC 30-60% 18-29% 5-17% <5% Entorhinal Parahippocampal Perirhinal Suzuki and Amaral, 1994

Take Home Message: All structures of the MTL appear to provide a similar complement of associative learning-related signals. There appears to be a conditionally dynamic relationship between different MTL structures such that depending on task demands different MTL structure can either contribute in similar/cooperative ways or in more clearly distinct way to mnemonic functions.

Location-Scene Association Task Gaffan (1994), Murray and Wise (1996), Murray et. al., (1998) ++ + New Scenes (n = 2-4) Fixation/ Baseline (300 ms) Scene/Target Presentation (500 ms) Delay (700 ms) Eye Movement Response

Probability Correct Behavioral Learning Curve and Delay Activity Over Time to Scene 653 Response (Spikes/Sec ) Baseline Activity Trials C Wirth et al., 2003

Probability Correct Behavioral Learning Curve and Delay Activity Over Time to Scene 386 Response (Spikes/Sec ) Trials Wirth et al., 2003

2 Categories of Changing Cells A. Sustained Changing cells: 56% of all changing cells B. Baseline Sustained Changing cells: 44% of all changing cells

What about the Perirhinal cortex? Yanike et al., 2008, In press

Selective Hippocampus (n = 2 monkeys) 89/145 (61 %) Changing Cells 25/89 (28%) Sustained Baseline Sustained PR Cortex (n = 2 monkeys) 83/128 (65 %) 26/83 (31%) 8/26 (31%) 18/26 (69%) 14/25 (56%) 11/25 (44%)

Yanike et al., 2008, In press

Object-Place Association Task Wirth et al, 2009 Fixation 500ms Cue 500ms Delay 700ms Early 500ms Late 500ms Reward ITI 2000ms Bar Release Period Fixation 500ms Cue 500ms Delay 700ms Early 500ms Late 500ms Reward ITI 2000ms Bar Release Period

Reward Release No Reward ITI Correct Trial Incorrect Trial Wirth et al, 2009

50% are outcome-selective Do hippocampal cells differentiate between correct and error trials?

Correct Up Cells N = 30 Error Up Cells N = 38 Wirth et al, 2009

Fixation 500ms Cue 500ms Delay 700ms Early 500ms Late 500ms Reward ITI 2000ms Bar Release Period Standard Trials Fixation Only Trials

Correct Up Cells N = 30 Error Up Cells N = 38 Wirth et al, 2009

Fixation 500ms Cue 500ms Delay 700ms Early 500ms Late 500ms Reward ITI 2000ms Bar Release Period Standard Trials Fixation Only Trials

Wirth et al, 2009

Correct Up Cells N = 30 Error Up Cells N = 38 Wirth et al, 2009

Object-Place Association Task Wirth et al, 2009 Fixation 500ms Cue 500ms Delay 700ms Early 500ms Late 500ms Reward ITI 2000ms Bar Release Period Fixation 500ms Cue 500ms Delay 700ms Early 500ms Late 500ms Reward ITI 2000ms Bar Release Period

Wirth et al, 2009

24/25/32 Pi Ia Id Ig Frontal LobeTemporal LobeInsular Cortex Cingulate Gyrus Parietal Lobe V4 23/29/30 7a/LIP STSdSTG TE STSv TEO 11/ DG Sub HPC 30-60% 18-29% 5-17% <5% Entorhinal Parahippocampal Perirhinal Suzuki and Amaral, 1994

Take Home Message: All structures of the MTL appear to provide a similar complement of associative learning-related signals. There appears to be a conditionally dynamic relationship between different MTL structures such that depending on task demands different MTL structure can either contribute in similar/cooperative ways or in more clearly distinct way to mnemonic functions.

Temporal Order Task 0.3 s0.9 s0.3 s0.5 s0.4 s 1.0 s> 4.0 s Encoding Phase Retrieval Phase 1st Cue2nd Cue 1st Choice2nd Choice Small Reward Large Reward s Pre-response Delay Inter-phase Delay Naya and Suzuki, SFN 2008

24/25/32 Pi Ia Id Ig Frontal LobeTemporal LobeInsular Cortex Cingulate Gyrus Parietal Lobe V4 23/29/30 7a/LIP STSdSTG TE STSv TEO 11/ DG Sub HPC 30-60% 18-29% 5-17% <5% Entorhinal Parahippocampal Perirhinal Suzuki and Amaral, 1994

Findings The most stimulus selective response are found in area TE and the perirhinal cortex. Perirhinal cortex has the strongest proportion of order and stimulus selective responses The hippocampus has the highest proportion of trial outcome selective responses.

Take Home Message: All structures of the MTL appear to provide a similar complement of associative learning-related signals. There appears to be a conditionally dynamic relationship between different MTL structures such that depending on task demands different MTL structure can either contribute in similar/cooperative ways or in more clearly distinct way to mnemonic functions.

Sylvia Wirth Marianna Yanike Emin Avsar

Eric Hargreaves Yuji Naya