Morphology and Physiology of Cortical Neurons in Layer I

Abstract

The electrophysiological and morphological properties of layer I neurons were studied in visual cortex slices from 7-to 19-dold rats using whole-cell recording and biocytin labeling. A heterogeneous population of small, nonpyramidal neurons was found. Approximately one third of the cells we recorded were neurogliaform cells; another third were multipolar neurons with axons descending out of layer I. The remaining cells were heterogeneous and were not classified. In slices from 7-to 10-d-old animals only, we identified Cajal-Retzius cells.Neurogliaform neurons had a very dense local axonal field, which was largely contained within layer I. Cells with descending axons had a relatively sparse local axonal arbor and projected at least to layer II and sometimes deeper. Spiking in neurogliaform neurons was followed by an afterdepolarizing potential, whereas spiking in cells with descending axons was followed by a slow after-hyperpolarizing potential (AHP). In addition, neurogliaform cells exhibited less spike broadening and a larger fast AHP after single spikes than did cells with descending axons. Generally, cells in layer I received synaptic inputs characterized as either GABA-or glutamate-mediated, suggesting the presence of excitatory and inhibitory inputs.With their output largely limited to layer I, neurogliaform cells could synapse with other layer I neurons, the most distal dendritic branches of pyramidal cells, or the dendrites of layer II/III interneurons, which invade layer I. Cells with descending axons could contact a wide variety of cortical cells throughout their vertical projection.

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

“…LCNs and DLPNs had the same resting membrane potential (Ϫ69.5 Ϯ 1.8 vs Ϫ65.3 Ϯ 1.6 mV; t test; p ϭ 0.13), input resistance (42.2 Ϯ 6.3 vs 60.0 Ϯ 12.5 m⍀; p ϭ 0.18) and generally fired relatively short duration action potentials (1.6 Ϯ 0.1 vs 1.9 Ϯ 0.3 msec; p ϭ 0.30). In comparison with young and juvenile layer 1 neurons (Hestrin and Armstrong, 1996;Zhou and Hablitz, 1996a), adult layer 1 neurons recorded in this study had a lower input resistance and a more hyperpolarized membrane potential, and they fired action potentials with shorter duration, which is consistent with the previous finding that postnatal maturation of intrinsic membrane properties of CNS neurons requires ϳ4 -6 weeks (Zhu, 2000;Perreault et al, 2003). The intrinsic firing properties were also investigated in these two types of layer 1 neurons.…”

“…As with previous in vitro studies (Hestrin and Armstrong, 1996;Chu et al, 2003), LCNs and DLPNs recorded in vivo display distinct intrinsic firing patterns. In particular, LCNs fire delayed action potentials in response to a near-threshold current pulse, which may contribute to the relatively slow initiation of whiskerevoked action potentials in these neurons (Fig.…”

“…All LCNs were multipolar, aspiny neurons, which were similar to neurogliaform neurons described previously (Kawaguchi, 1995;Hestrin and Armstrong, 1996;Gupta et al, 2000). These neurons had an axon ramifying densely within layer 1.…”

A Novel Type of GABAergic Interneuron Connecting the Input and the Output Regions of the Hippocampus

“…CR cells in the hippocampus, like their counterparts in layer 1 of the neocortex (Marin-Padilla, 1984;Ogawa et al, 1995;Hestrin and Armstrong, 1996;Del Río et al, 1997), are likely to play an important role in development. They may serve as a template for lamina-specific ingrowth of entorhinal fibers and seem to disappear in the early postnatal period after the arrival of these fibers (Del Río et al, 1996).…”

“…They may serve as a template for lamina-specific ingrowth of entorhinal fibers and seem to disappear in the early postnatal period after the arrival of these fibers (Del Río et al, 1996). The GABAergic interneurons in the OML described in the present paper are unlikely to represent CR cells: (1) OML interneurons have a multipolar dendritic configuration and an extensive axonal network; in contrast, CR cells are characterized by a bipolar shape, often with only a single dendritic process and an immature axon, both oriented tangentially to the pial surface or the hippocampal fissure (von Haebler et al, 1993;Del Río et al, 1996, 1997; (2) OML interneurons are positive for GAD, whereas CR cells may be glutamatergic (Del Río et al, 1995) or GABAergic (Martin et al, 1989); (3) OML interneurons generate high-frequency trains of brief action potentials on sustained current injection, whereas CR cells fire lowfrequency trains of spikes of much longer duration (von Haebler et al, 1993;Hestrin and Armstrong, 1996); (4) OML interneurons were recorded in slices from animals ranging in age from P10 -P31 in the present study. In contrast, many CR cells already have disappeared at that time and most of the remaining CR cells undergo degeneration (von Haebler et al, 1993; Del Río et al, 1997).…”