Timing of Single-Neuron and Local Field Potential Responses in the Human Medial Temporal Lobe

Abstract

Summary The relationship between the firing of single cells and local field potentials (LFPs) has received increasing attention, with studies in animals [1-11] and humans [12-14]. Recordings in the human medial temporal lobe (MTL) have demonstrated the existence of neurons with selective and invariant responses [15], with a relatively late but precise response onset around 300 ms after stimulus presentation [16-18] and firing only upon conscious recognition of the stimulus [19]. This represents a much later onset than expected from direct projections from inferotemporal cortex [16, 18]. The neural mechanisms underlying this onset remain unclear. To address this issue, we performed a joint analysis of single-cell and LFP responses during a visual recognition task. Single-neuron responses were preceded by a global LFP deflection in the theta range. In addition, there was a local and stimulus-specific increase in the single-trial gamma power. These LFP responses correlated with conscious recognition. The timing of the neurons’ firing was phase locked to these LFP responses. We propose that whereas the gamma phase locking reflects the activation of local networks encoding particular recognized stimuli, the theta phase locking reflects a global activation that provides a temporal window for processing consciously perceived stimuli in the MTL.

Scene-selective coding by single neurons in the human parahippocampal cortex

“…This difference in response latency between unit activity and LFP confirms the notion that neuronal action potentials represent the output activity of a neuron, whereas the LFP represents postsynaptic input activity and ongoing neuronal processing (20). These findings are in line with previous reports that LFP responses precede the onset of single-cell firing in the human MTL (26).…”

Hippocampal gamma‐band Synchrony and pupillary responses index memory during visual search

“…Studies of memory‐related hippocampal physiology in rodents typically examine spike‐field synchrony and in a specific segment of a specific hippocampal subfield, most often the septal (“dorsal”) CA1. In humans, measures of medial‐temporal lobe gamma synchrony or oscillatory activity typically use power (but see (Jacobs et al, ; Rey et al, ); localization is approximate and often collapsed across hippocampal subfield, the septotemporal axis, and sometimes larger regions of medial temporal lobe. Furthermore, primate studies typically measure subsequent memory effects (or “difference because of memory”) rather than recall (but see Sederberg et al, ; Rutishauser et al, ; Kucewicz et al, ).…”

More than spikes: common oscillatory mechanisms for content specific neural representations during perception and memory

“…Several studies have bridged the gap from single neurons to content-specific patterns in the LFP, showing both category [21,22] and stimulus [23,24] specific neuronal firing and LFP responses at low (below 10 Hz) and high (>30 Hz) frequencies in the human temporal lobe. Thus, activity in the theta and gamma bands appear particularly relevant for neural representation [25] (Figure 1A).…”

“…Content-specific neurons fire at specific frequencies, but across an extended and therefore unspecific phase range. Content specific information (right panel) in this scenario can be recovered via frequency-specific power increases or by considering neuronal firing as a function of power [22,24,25,27,31]. C) Layout similar to B for a phase-specific firing scheme.…”

“…First, low-frequency oscillations convey unique information about sensory stimuli between adjacent frequencies [27]. Both neuronal firing and gamma responses may be locked to specific phases of low-frequency oscillations [24,45], contributing to phase-amplitude coupling (PAC) between low-frequency phase and gamma amplitude [10]. In turn, spiking and PAC exhibits the diversity of frequencies and phases necessary for a frequency and phase-dependent coding scheme [33,36,46,47] (Figure 1D).…”