The postsubiculum and spatial learning: the role of postsubicular synaptic activity and synaptic plasticity in hippocampal place cell, object, and object-location memory

TY - JOUR

T1 - The postsubiculum and spatial learning

T2 - the role of postsubicular synaptic activity and synaptic plasticity in hippocampal place cell, object, and object-location memory

AU - Bett, David

AU - Stevenson, Cassie H.

AU - Shires, Kate L.

AU - Smith, Michael T.

AU - Martin, Stephen J.

AU - Dudchenko, Paul A.

AU - Wood, Emma R.

PY - 2013/4/17

Y1 - 2013/4/17

N2 - Visual landmarks exert stimulus control over spatial behavior and the spatially tuned firing of place, head-direction, and grid cells in the rodent. However, the neural site of convergence for representations of landmarks and representations of space has yet to be identified. A potential site of plasticity underlying associations with landmarks is the postsubiculum. To test this, we blocked glutamatergic transmission in the rat postsubiculum with CNQX, or NMDA receptor-dependent plasticity with d-AP5. These infusions were sufficient to block evoked potentials from the lateral dorsal thalamus and long-term depression following tetanization of this input to the postsubiculum, respectively. In a second experiment, CNQX disrupted the stability of rat hippocampal place cell fields in a familiar environment. In a novel environment, blockade of plasticity with d-AP5 in the postsubiculum did not block the formation of a stable place field map following a 6 h delay. In a final behavioral experiment, postsubicular infusions of both compounds blocked object-location memory in the rat, but did not affect object recognition memory. These results suggest that the postsubiculum is necessary for the recognition of familiar environments, and that NMDA receptor-dependent plasticity in the postsubiculum is required for the formation of new object-place associations that support recognition memory. However, plasticity in the postsubiculum is not necessary for the formation of new spatial maps.

AB - Visual landmarks exert stimulus control over spatial behavior and the spatially tuned firing of place, head-direction, and grid cells in the rodent. However, the neural site of convergence for representations of landmarks and representations of space has yet to be identified. A potential site of plasticity underlying associations with landmarks is the postsubiculum. To test this, we blocked glutamatergic transmission in the rat postsubiculum with CNQX, or NMDA receptor-dependent plasticity with d-AP5. These infusions were sufficient to block evoked potentials from the lateral dorsal thalamus and long-term depression following tetanization of this input to the postsubiculum, respectively. In a second experiment, CNQX disrupted the stability of rat hippocampal place cell fields in a familiar environment. In a novel environment, blockade of plasticity with d-AP5 in the postsubiculum did not block the formation of a stable place field map following a 6 h delay. In a final behavioral experiment, postsubicular infusions of both compounds blocked object-location memory in the rat, but did not affect object recognition memory. These results suggest that the postsubiculum is necessary for the recognition of familiar environments, and that NMDA receptor-dependent plasticity in the postsubiculum is required for the formation of new object-place associations that support recognition memory. However, plasticity in the postsubiculum is not necessary for the formation of new spatial maps.

KW - 2-Amino-5-phosphonovalerate/pharmacology

KW - 6-Cyano-7-nitroquinoxaline-2,3-dione/pharmacology

KW - Action Potentials/drug effects

KW - Animals

KW - Conditioning, Operant/drug effects

KW - Excitatory Amino Acid Antagonists/pharmacology

KW - Excitatory Postsynaptic Potentials/drug effects

KW - Exploratory Behavior/drug effects

KW - Hippocampus/cytology

KW - Learning/physiology

KW - Male

KW - Neural Pathways/drug effects

KW - Neuronal Plasticity/drug effects

KW - Neurons/drug effects

KW - Photic Stimulation

KW - Rats

KW - Recognition (Psychology)

KW - Spatial Behavior/drug effects

KW - Visual Perception/drug effects

U2 - 10.1523/JNEUROSCI.5476-12.2013

DO - 10.1523/JNEUROSCI.5476-12.2013

M3 - Article

C2 - 23595751

SN - 0270-6474

VL - 33

SP - 6928

EP - 6943

JO - Journal of Neuroscience

JF - Journal of Neuroscience

IS - 16

ER -