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J Neurophysiol 89: 2176-2184, 2003. First published November 20, 2002; doi:10.1152/jn.01033.2002
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J Neurophysiol (April 1, 2003). 10.1152/jn.01033.2002
Submitted on Submitted 24 May 2002; accepted in final form 18 November 2002

Amygdala Input Promotes Spread of Excitatory Neural Activity From Perirhinal Cortex to the Entorhinal-Hippocampal Circuit

Riichi Kajiwara,1 Ichiro Takashima,1 Yuka Mimura,1 Menno P. Witter,2 and Toshio Iijima1,3

 1Neuroscience Research Institute, National Institute of Advanced Industrial Science and Technology, 1-1-1 Umezono, Tsukuba 305-8568, Japan;  2Graduate School Neurosciences Amsterdam, Research Institute Neurosciences, Department of Anatomy, Vrije Universiteit Medical Center, Van der Boechorststraat 7, 1081 BT Amsterdam, The Netherlands; and  3Systems Neuroscience, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba, Sendai 980-8577, Japan

Kajiwara, Riichi, Ichiro Takashima, Yuka Mimura, Menno P. Witter, and Toshio Iijima. Amygdala Input Promotes Spread of Excitatory Neural Activity From Perirhinal Cortex to the Entorhinal-Hippocampal Circuit. J. Neurophysiol. 89: 2176-2184, 2003. A number of sensory modalities most likely converge in the rat perirhinal cortex. The perirhinal cortex also interconnects with the amygdala, which plays an important role in various motivational and emotional behaviors. The neural pathway from the perirhinal cortex to the entorhinal cortex is considered one of the main paths into the entorhinal-hippocampal network, which has a crucial role in memory processes. To investigate the potential associative function of the perirhinal cortex with respect to sensory and motivational stimuli and the influence of the association on the perirhinal-entorhinal-hippocampal neurocircuit, we prepared rat brain slices including the perirhinal cortex, entorhinal cortex, hippocampal formation, and amygdala. We used an optical imaging technique with a voltage-sensitive dye to analyze 1) the spatial and functional distribution of inputs from the lateral nucleus of the amygdala to the perirhinal cortex; 2) the spread of neural activity in the perirhinal cortex after layers II/III stimulation, which mimics sensory input to the perirhinal cortex; and 3) the effect of associative inputs to the perirhinal cortex from both the lateral amygdaloid nucleus and layers II/III of the perirhinal cortex on the perirhinal-entorhinal-hippocampal neurocircuit. Following stimulation in the superficial layers of the perirhinal cortex, electrical activity only propagated into the entorhinal cortex when sufficient activation occurred in the deep layers of perirhinal area 35. We observed that single stimulation of either the perirhinal cortex or amygdala did not result in sufficient neural activation of the deep layers of areas 35 to provoke activity propagation into the entorhinal cortex. However, the deep layers of area 35 were depolarized much more strongly when the two stimuli were applied simultaneously, resulting in spreading activation in the entorhinal cortex. Our observations suggest that a functional neural basis for the association of higher-order sensory inputs and emotion-related inputs exists in the perirhinal cortex and that transfer of sensory information to the entorhinal-hippocampal circuitry might be affected by the association of that information with incoming information from the amygdala.




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