Physiological Properties of Macaque V1 Neurons are Correlated With Extracellular Spike Amplitude, Duration, and Polarity

Abstract

In the lateral geniculate nucleus (LGN) the large neurons of the magnocellular layers are functionally distinct and anatomically segregated from the small neurons of the parvocellular layers. This segregation of large and small cells is not maintained in the primary visual cortex (V1); instead a heterogeneous mixture of cells occurs, particularly in the output layers. Nevertheless, our results indicate that for the middle and upper layers of V1, cell size remains a predictor of physiological properties. We recorded extracellularly from neurons in V1 of alert monkeys and analyzed the amplitude, duration, and polarity of the action potentials of 199 cells. Of 156 cells that could be assigned to specific cortical layers, 137 (88%) were localized to the middle and upper cortical layers, layer 4 and above. We summarize evidence that the large-amplitude spikes are discharged by large cells, whereas small-amplitude spikes are the action potentials of smaller cells. Large spikes were predominantly negative and of longer duration, whereas small spikes were predominantly positive and briefer. The putative large cells had lower ongoing activity, smaller receptive field activating regions and higher selectivity for stimulus geometry and stimulus motion than the small cells. The contrasting properties of the large and the small cells were illustrated dramatically in simultaneous recordings made from adjacent cells. Our results imply that there may be an anatomic pairing or clustering of small and large cells that could be integral to the functional organization of the cortex. We suggest that the small and the large cells of area V1 have different roles, such that the small cells may shape the properties of the large output cells. If some of the small cells are also output cells, then cell size should be a predictor of the type of information being sent to other brain regions. Because of their high activity and relative ease of stimulation, the small cells also may contribute disproportionately to in vivo images based on metabolic responses such as changes in blood flow.

Trade-Off between Object Selectivity and Tolerance in Monkey Inferotemporal Cortex

“…Previous studies performed in cortical slices and anesthetized animals (McCormick et al, 1985;Connors and Gutnick, 1990;Nowak et al, 2003) and additional studies based on cross-correlation analysis of spike trains (Bartho et al, 2004;Tamura et al, 2004) have shown the reliability of such an approach in identifying neuronal typing. As a consequence, many authors have distinguished between putative excitatory and inhibitory neurons recorded in different brain areas of awake animals (such as hippocampus, somatosensory cortex, lower and higher visual cortical areas, and rat barrel cortex) using only the temporal features of the spike waveforms (Mountcastle et al, 1969;Gur et al, 1999;Frank et al, 2001;Bruno and Simons, 2002;Andermann et al, 2004;Mitchell et al, 2007). In this study, following Bruno and Simons (2002), two components of the waveform were taken as distinctive features of the neuron type: (1) the duration (width) of the central peak (negative or positive); and (2) the width of the following trough (corresponding to the spike afterhyperpolarization).…”

“…To examine this, the recorded neuronal population was divided into putative inhibitory and excitatory neurons based on extracellular measures of excitatory and inhibitory neuronal typing suggested previously (Mountcastle et al, 1969;Gur et al, 1999;Frank et al, 2001;Bruno and Simons, 2002;Constantinidis and Goldman-Rakic, 2002;Swadlow, 2003;Andermann et al, 2004;Hasenstaub et al, 2005;Mitchell et al, 2007) (Fig. 5A).…”

Selectivity of Canary HVC Neurons for the Bird's Own Song: Modulation by Photoperiodic Conditions

“…As in previous in vivo intracellular and extracellular studies (Mooney, 2000;Mooney et al, 2001;Hahnloser et al, 2002;Rauske et al, 2003), we distinguished putative HVC relay cells and putative HVC interneurons based on the spike waveform of the recorded cells. Classically, the spike amplitude is defined as the voltage difference between the peak of the negativity and the peak of the positivity that follows it; the spike width is the duration between the beginning of the negativity and the peak of the following positive wave (Wilson et al, 1994;Gur et al, 1999;Henze et al, 2000;Del Negro and Edeline, 2002). Spike parameters were always analyzed blind to the photoperiod conditions of the bird and blind to the responses obtained during the experiment.…”

Monkey Prefrontal Cortical Pyramidal and Putative Interneurons Exhibit Differential Patterns of Activity Between Prosaccade and Antisaccade Tasks

“…In the PFC, such studies in monkeys have implicated interneurons in tuning of spatial memory fields (Wilson et al, 1994;Rao et al, 1999Rao et al, , 2000Constantinidis and Goldman-Rakic, 2002;Wang et al, 2004) and abstract numerical categories (Diester and Nieder, 2008). Such an approach has also been successful in somatosensory (Mountcastle et al, 1969;Simons, 1978;McCormick et al, 1985), motor (Merchant et al, 2008), and visual cortex (Gur et al, 1999;Mitchell et al, 2007). Recently, we reported that PFC neurons showed task selectivity in a paradigm in which monkeys were required to alternate between blocks of prosaccade trials, in which they were required to generate a saccade to a flashed visual stimulus, and antisaccade trials (Hallett, 1978;Munoz and Everling, 2004), in which they were required to generate a saccade to the mirror location (Everling and DeSouza, 2005;Johnston and Everling, 2006b;Johnston et al, 2007).…”