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 = 31 1). (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. The rsp cells comprised both nPP and PP neurons and had heterogenous electrophysiological properties. 5. Bursting neurons (21.7% of all cells) were recorded at cortical depths between 900 and 1,300 mum with features indicative of intrinsic mechanisms of burst generation. Bursts were composed of more than three action potentials of >250 Hz riding on a depolarizing envelope. A transient, low-threshold inward conductance was observed synchronously with the depolarizing envelope of bursts. 6. Two distinct subgroups of bursting neurons were identified according to their intraburst firing pattern. In 60 ib class i cells, the action potentials were relatively slow (see details in the companion paper), did not have well-developed fast afterhyperpolarizations (fAHPs), and were gradually inactivated within a burst. In 79 other nib class ii cells, bursts were composed of noninactivating, relatively fast, serial action potentials with well-developed fAHPs. PP and VL stimulation evoked monosynaptic EPSPs and excitatory-inhibitory postsynaptic potentials (E-IPSPs) in both ib/nPP and nib/nPP cells. Monosynaptic EPSPs were observed in significantly more nib than ib/nPP cells. Similar ratios of responses were found in fPP versus sPP neurons. 7. Fast-spiking (class iii) neurons had a high-frequency, nonaccommodative firing pattern and very fast action potentials (0.25 +/-0.03 ms, mean +/- SD, width at half-amplitude) with large fAHPs and a characteristic lack of slow after hyperpolarizations (sAHPs, type III spikes, defined in the companion paper). The primary slope (516 +/- 86 Hz/nA) of spike frequency versus current intensity (f-I) relationships in fsp cells was significantly higher than in other neurons. Most fsp cells displayed vivid, frequently subthreshold background activity resembling synaptic potentials superimposed on the membrane potential. Weak PP stimulation produced only monosynaptic EPSPs in >95% of fsp/nPP cells, as opposed to VL stimulation (<40%). Stimulation of VL evoked fast-rising and decaying monosynaptic EPSPs followed by oligo-synaptic IPSPs in most fsp cells. Strong PP stimulation evoked monosynaptic EPSPs of long duration, which initiated characteristically long series of high-frequency action potentials in most fsp cells. In a smaller portion of fsp neurons, strong PP stimulations also elicited polysynaptic IPSPs after the initial monosynaptic EPSPs. The results suggest that most fsp/nPP cells were inhibitory interneurons located within recurrent collateral PP pathways. 8. Regular-spiking (class iv) neurons were found at all cortical depths, and represented the majority (69%) of recorded cells. The rsp cells showed no bursting firing pattern at any membrane potential and displayed prominent accommodation of firing activity as opposed to fsp cells. Graphs of f-I relationships in rsp cells revealed a primary slope of 196 +/- 32 Hz/nA that was significantly slower than that in fsp cells. Both VL and PP stimulation evoked monosynaptic EPSPs or E-IPSPs in rsp cells. 9. It is concluded that neurons in the motor cortex of conscious cats have characteristic differences in firing activity and synaptic response properties that warrant their functional separation into at least four cell classes that may operate differently in the neocortical circuits.
