Crossed-corticostriatal (CCS) cells, which innervate both sides of the striatum ( Wilson, 1987 Lei et al., 2004), are another prominent subtype of L5 pyramidal neuron. One prominent subtype, corticopontine (CPn) neurons, issues collaterals to the ipsilateral striatum (the input nucleus of the basal ganglia) and pontine nuclei, which provide innervation to the cerebellum. In the frontal cortex, L5 pyramidal cells comprise multiple subtypes that can be segregated by their external projections. Previously, we found that cells in various thalamic nuclei are diverse in their preferred timing of action potential generation during Up/Down cycles ( Ushimaru et al., 2012) neurons in thalamic nuclei receiving input from the basal ganglia, and neurons in the reticular (Rt) nucleus, exhibit increases in activity during the transition from Down- to Up-states, while those receiving input from the cerebellum exhibit more temporally distributed activity. Up-states in SWs are thought to be initiated by activity in layer 5 (L5) pyramidal cells ( Sanchez-Vives and McCormick, 2000 Chauvette et al., 2010 Lőrincz et al., 2015), but thalamic activity may also contribute to the SW generation ( Crunelli and Hughes, 2010 David et al., 2013 Lemieux et al., 2014). For this synaptic modification to occur, the neocortex is thought to interact with multiple memory subsystems within the hippocampus, basal ganglia, and cerebellum. During SWs, the strengths of synaptic connections are modified to restructure cortical circuits in response to previous experiences occurring during awake states ( Louie and Wilson, 2001 Euston et al., 2007). Gamma-band (30–80 Hz) oscillations are nested within Up-states ( Valencia et al., 2013), and GABAergic fast-spiking (FS) cells are essential for their generation ( Buzsáki and Draguhn, 2004 Sohal et al., 2009). The neocortex exhibits two major activity states: a slow-wave (SW) state in which neurons fluctuate between hyperpolarized “Down-states” and depolarized “Up-states” occurring at low frequencies, and a continuously depolarized state. Together, these findings reveal a temporally ordered pattern of output from diverse neuron subtypes in the frontal cortex and related thalamic nuclei during neocortical oscillations. At the start of slow-wave depolarizations, activity in thalamic neurons receiving inhibition from the basal ganglia occurred earlier than activity in cortical neurons. Within gamma cycles nested in the slow-wave depolarization, cortical pyramidal cells fired earlier than did interneurons. We found that the timing of action potentials during slow waves in individual cortical neurons was correlated with their laminar positions and axonal targets. SIGNIFICANCE STATEMENT Patterned activity in neocortical electroencephalograms, including slow waves and gamma oscillations, is thought to reflect the organized activity of neocortical neurons that comprises many specialized neuron subtypes. In addition to Up-state firing specificity, CCS and CPn cells exhibited differences in activity during cortical desynchronization, further indicating projection- and state-dependent information processing within L5. These results suggest that thalamic and cortical pyramidal neurons are activated in a specific temporal sequence during Up/Down cycles, but cortical pyramidal cells are activated at a similar gamma phase. Activity in some FS, CCS, and CPn neurons occurred in phase with Up-nested gamma rhythms, with FS neurons showing phase delay relative to pyramidal neurons. During the transition from Down- to Up-states, increased activity in these neurons was highly temporally structured, with spiking occurring first in thalamocortical neurons, followed by cortical FS cells, CCS cells, and, finally, CPn cells. Here we compare the in vivo firing patterns of corticopontine (CPn) pyramidal cells, crossed-corticostriatal (CCS) pyramidal cells, and fast-spiking (FS) GABAergic neurons in the rat frontal cortex, with those of thalamocortical neurons during Up/Down cycles in the anesthetized condition. Depolarizing Up-states involve activity in layer 5 (L5) of the neocortex, but it is unknown how diverse subtypes of neurons within L5 participate in generating and maintaining Up-states. Slow-wave oscillations, the predominant brain rhythm during sleep, are composed of Up/Down cycles.
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