Bidirectional synaptic changes in deep and superficial hippocampal neurons followingin vivoactivity

Abstract

Neuronal activity during experience is thought to induce plastic changes within the hippocampal network which underlie memory formation, although the extent and details of such changes in vivo remain unclear. Here, we employed a temporally precise marker of neuronal activity, CaMPARI2, to label active CA1 hippocampal neurons in vivo, followed by immediate acute slice preparation and electrophysiological quantification of synaptic properties. Recently active neurons in the superficial sublayer of stratum pyramidale displayed larger post-synaptic responses at excitatory synapses from area CA3, with no change in pre-synaptic release probability. In contrast, in vivo activity weakened both pre- and post-synaptic excitatory weights onto pyramidal cells in the deep sublayer. In vivo activity of deep and superficial neurons within sharp-wave ripples was bidirectionally changed across experience, consistent with the observed changes in synaptic weights. These findings reveal novel, fundamental mechanisms through which the hippocampal network is modified by experience to store information.

Circuit dynamics of superficial and deep CA1 pyramidal cells and inhibitory cells in freely-moving macaques

“…Because macaques also show extra-hippocampal projec�ons that are organized by CA1 pyramidal depth 81,82 , this suggests separable hippocampo-cor�cal networks may be organized through parallel channels within primate CA1. These findings, together with strata-specific differences in experience-dependent plas�city and in memory forma�on 15,21,22,83,84 , suggest that their detec�on in primates may prove to be key to understanding how the hippocampus structures ac�vity during memory forma�on.…”

“…Based on studies in rats and mice, these dynamics arise from a well-described and diverse range of cell classes [8][9][10][11] . For example, the pyramidal cell layer is organized into radial-axis strata 12 , each receiving dis�nct afferents [13][14][15][16] , bearing different intrinsic and taskrelated response characteris�cs 15,[17][18][19][20][21][22][23] , and projec�ng to different target structures 12,22 . The dynamics of these pyramidal cells are precisely regulated by inhibitory cell classes 10,24,25 that differ from each other in their behaviorally-specific firing paterns and roles in shaping network oscilla�ons 11,[26][27][28][29][30] .…”

Development of differential sublaminar feedforward inhibitory circuits in CA1 hippocampus requiresSatb2

“…Although diverse, CA1 PCs can be broadly split into two classes based on the radial position of their soma within the stratum pyramidale as deep (closer to the stratum oriens) and superficial (closer to the stratum radiatum) 1 . In mice, deep and superficial PCs exhibit distinct activity patterns during spatial navigation tasks and network oscillations necessary for learning and memory [7][8][9][10][11][12][13][14][15] . Recent work shows that biases in connectivity and physiology of synapses between inhibitory interneurons and deep versus superficial PCs likely play an important role in their differential activity [16][17][18] .…”