Rapid Arrival and Integration of Ascending Sensory Information in Layer 1 Nonpyramidal Neurons and Tuft Dendrites of Layer 5 Pyramidal Neurons of the Neocortex

Abstract

Ascending sensory inputs arriving in layer 1 of the neocortex carry crucial signals for detecting salient information; but how the inputs are processed in layer 1 is unknown. Using a whole-cell in vivo recording technique targeting nonpyramidal neurons in layer 1 and tuft dendrites of layer 5 pyramidal neurons in layers 1-2, we examined the processing of these ascending sensory inputs in the barrel cortex. Here, we show that local circuit and deeper-layer-projecting neurons in layer 1, as well as tuft dendrites and somata of layer 5 pyramidal neurons, respond to multiple whiskers (6 -15) with robust EPSPs. Remarkably, the latency for primary whisker-evoked responses is as short as ϳ5-7 msec in layer 1 neurons and tuft dendrites of layer 5 pyramidal neurons. In addition, the latency for primary whiskerevoked responses in tuft dendrites of layer 5 pyramidal neurons is ϳ1 msec shorter than that in somata. These results indicate that ascending sensory inputs arrive in layers 1 and 4 concurrently, which provides a neural mechanism for rapid integration and coincident detection of salient sensory information.

Differential Expression ofIAChannel Subunits Kv4.2 and Kv4.3 in Mouse Visual Cortical Neurons and Synapses

“…In rat somatosensory cortex, layer 1 dendrites and interneurons receive short-latency inputs from whiskers, which elicit Ca 2ϩ action potentials (Larkum and Zhu, 2002;Zhu and Zhu, 2004). Similar responses were found after stimulation of excitatory inputs to thin distal dendrites of CA1 pyramidal neurons (Cai et al, 2004;Losonczy and Magee, 2006).…”

Chandelier Cells Control Excessive Cortical Excitation: Characteristics of Whisker-Evoked Synaptic Responses of Layer 2/3 Nonpyramidal and Pyramidal Neurons

“…In one FS neuron, the shortest latency initial EPSP was evoked by a first-order surrounding whisker; the amplitude of that whisker-evoked EPSP was the second largest in the cell. Unlike other FS neurons (Zhu and Connors, 1999;Margrie et al, 2003;Zhu and Zhu, 2004), chandelier cells responded to whisker stimulation with a small, long-latency initial EPSP followed by several delayed EPSPs (Figs. 1C,D,2A,B).…”

“…The average responses in these neurons to the deflection of first-order and second-order surrounding whiskers are ϳ50% of those to the deflection of the primary and first-order surrounding whiskers, respectively; however, the receptive field structure of cortical inhibitory interneurons, which represent a significant population of cortical neurons and may participate in various cortical functions (Peters and Jones, 1984;Kawaguchi and Kubota, 1997;Somogyi et al, 1998), is much less understood (Zhu and Connors, 1999;Bruno and Simons, 2002;Swadlow and Gusev, 2002). This is further complicated by recent evidence that distinct inhibitory interneurons may possess different receptive field properties (Hirsch et al, 2003;Zhu and Zhu, 2004).…”

Ultrastructural analysis of projections to the pulvinar nucleus of the cat. I: Middle suprasylvian gyrus (areas 5 and 7)

“…In turn, thalamocortical projections to layer I have been shown to be very effective in activating layer V cells in the rat (Zhu and Zhu, 2004). However, layer IV inputs can also activate layer V cells by means of contacts on their apical dendrites and it has been proposed that layer V cells could act to detect the coincidence of thalamocortical activation arriving in layers IV and I (Zhu and Zhu, 2004). Alternatively, layer IV pulvinocortical inputs may primarily target the apical dendritic tufts of layer VI corticothalamic cells (Tömböl et al, 1975;Bourassa et al, 1995).…”

“…The apical dendrites of layer V cells can reach layer I forming an extensive tuft (Valverde, 1971;Deschênes et al, 1994). In turn, thalamocortical projections to layer I have been shown to be very effective in activating layer V cells in the rat (Zhu and Zhu, 2004). However, layer IV inputs can also activate layer V cells by means of contacts on their apical dendrites and it has been proposed that layer V cells could act to detect the coincidence of thalamocortical activation arriving in layers IV and I (Zhu and Zhu, 2004).…”