Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat. I. Patterns of firing activity and synaptic responses

Abstract

1. Patterns of firing activity and characteristics of antidromic and synaptic responses to stimulation of the pyramidal tract at peduncular level [peduncular pyramidal tract (PP)] and the ventrolateral thalamic nucleus (VL) were studied in neurons of area 4 gamma of the motor cortex of awake, chronic cats using intracellular microelectrode techniques. The results offer a new functional classification of neocortical neurons based on electrophysiological properties of the 640 recorded cells. 2. Four classes of neurons were distinguished: (class i) inactivating bursting (ib) neurons (n = 60) including fast antidromic response PP (fPP) (n = 0), slow antidromic response PP (sPP) (n = 11), and no antidromic response PP cells (nPP) (n = 49); (class ii) noninactivating bursting (nib) neurons (n = 79), including fPP (n = 23), sPP (n = 0), and nPP cells (n = 56); (class iii) fast-spiking (fsp) neurons (n = 56), including fPP (n = 0), sPP (n = 0), and nPP cells (n = 56); and (class iv) regular-spiking (rsp) neurons (n = 445), including fPP (n = 96), sPP (n = 38), and nPP cells (n = 311). (Neurons in each classification were further separated by their antidromic responses to PP stimulation: fast PP (fPP) slow PP (sPP), or nPP cells, the latter not responding antidromically to electrical stimulation of the peduncle.) 3. Recurrent monosynaptic excitatory postsynaptic potentials (EPSPs) followed antidromic spikes elicited by PP stimulation in most (96%) fPP but much fewer (24%) sPP cells. In fPP cells, it was possible to separate the PP EPSPs into two monosynaptic EPSP components that were generated by other fPP and sPP cells, respectively. VL stimulation evoked monosynaptic EPSPs in 100% of fPP cells (vs. 63% of sPP cells) and antidromic action potentials in 16% of fPP cells (vs. 12% of sPP cells). 4. Firing activity consisted of single spike discharges in most PP cells; however, noninactivating bursting was observed in 19% of fPP cells, and inactivating bursting was observed in 23% of sPP cells (see below). In 18% of ib and 11% of nib/nPP neurons, VL stimulation elicited antidromic action potentials. Other bursting neurons proved to be PP cells with characteristic differences in axonal conduction velocity (see above). All PP cells among the nib cells were fPP, and all PP cells among the ib cells were sPP cells. All fsp neurons were found to be nPP cells, and none could be activated antidromically by VL stimulation. Thus the fsp pattern of discharge distinguished a unique class of nPP cells.(ABSTRACT TRUNCATED AT 400 WORDS)

Differential Involvement of Excitatory and Inhibitory Neurons of Cat Motor Cortex in Coincident Spike Activity Related to Behavioral Context

“…1C) so as to avoid inaccuracies that may arise from difficulties in determining the point of initial deviation from the baseline that has been previously reported (Constantinidis and Goldman-Rakic, 2002). Bursting behavior has been shown to occur in a subset of cortical neurons, and these neurons rarely show extracellular firing patterns that are particularly distinctive of either RS or FS subtypes (Calvin and Sypert, 1976;Baranyi et al, 1993;Bair et al, 1994). However, these neurons have been shown to be identifiable by computing and plotting the logarithm of each neuron's interspike interval (ISI) distribution (Nowak et al, 2003).…”

Distribution and Kinetic Properties of GABAergic Inputs to Layer V Pyramidal Cells in Rat Auditory Cortex

“…In current clamp studies, IB cells appear to have predominantly excitatory responses to stimulation of thalamocortical inputs, while RS cells have mixed excitatory and inhibitory responses (Chagnac-Amitai and Connors 1989;Baranyi et al 1993;Nunez et al 1993;Nicoll et al 1996;Hefti and Smith 2000;Schubert et al 2001). However, electron microscopic evidence is at odds with this physiological finding in the somatosensory cortex.…”

Inferring network activity from synaptic noise

“…During such activity, the EEG, as an indicator of population activity, shows low-amplitude fast fluctuations (''desynchronized EEG'') [91]. Intracellular recordings in the cortex of awake animals or under anesthesia (such as ketamine-xylazine or barbiturate) paralleled with EEG recordings, aiming at the characterization of the cellular activity during such EEG-activated states, date back to over 30 years ago [2,3,6,8,60,67,91,92,110] (for reviews see [23,90]). They found, that the intense synaptic inputs due to network activity result in seemingly random fluctuations of the membrane potential.…”

“…2A, right). Furthermore, the large number of synaptic inputs maintains the membrane in a high-conductance state with fluctuating and low input resistance [2,3,6,60,90,110] (typically, about 12 MX compared to about 60 MX in quiescent conditions; Fig. 2C and D, right), resulting in small membrane time constants of the order of about 4 ms [22,23].…”

“…Under these conditions, the membrane potential (V m ) of cortical neurons is depolarized (average V $ À65 mV compared to V $ À80 mV in quiescent states without synaptic noise) and shows high-amplitude fluctuations (V m standard deviation r V around 4 mV). In addition, this intense synaptic activity sets the cellular membrane into a high-conductance state, in which the input resistance is reduced by 3 to 5 times compared to quiescent states [2,3,8,23,67].…”