Short duration waveforms recorded extracellularly from freely moving rats are representative of axonal activity

Abstract

While extracellular somatic action potentials from freely moving rats have been well characterized, axonal activity has not. We report direct extracellular tetrode recordings of putative axons whose principal feature is a short duration waveform (SDW) with an average peak-trough length less than 179 μs. While SDW recordings using tetrodes have previously been treated as questionable or classified as cells, we hypothesize that they are representative of axonal activity. These waveforms have significantly shorter duration than somatic action potentials, are triphasic and are therefore similar to classic descriptions of microelectrode recordings in white matter and of in vitro action potential propagation along axons. We describe SDWs recorded from pure white-matter tracts including the alveus and corpus callosum. Recordings of several SDWs in the alveus exhibit grid-like firing patterns suggesting these axons carry spatial information from entorhinal cortical neurons. Finally, we locally injected the GABAA agonist Muscimol into layer CA1 of the hippocampus while simultaneously recording somatic activity and SDWs on the same tetrodes. The persistent activity of SDWs during Muscimol inactivation of somatic action potentials indicates that SDWs are representative of action potential propagation along axons projecting from more distal somata. This characterization is important as it illustrates the dangers of exclusively using spike duration as the sole determinant of unit type, particularly in the case of interneurons whose peak-trough times overlap with SDWs. It may also allow future studies to explore how axonal projections from disparate brain regions integrate spatial information in the hippocampus, and provide a basis for studying the effects of pharmaceutical agents on signal transmission in axons, and ultimately to aid in defining the potential role of axons in cognition.

Large-scale recording of thalamocortical circuits: in vivo electrophysiology with the two-dimensional electronic depth control silicon probe

“…These putative axonal spikes had short durations (Fig. 5E) and a triphasic characteristic, which is in agreement with the results obtained by Robbins et al (2013).…”

Global dynamics of selective attention and its lapses in primary auditory cortex

“…Below the averaged spike waveform in Figure 6a, the histogram shows the distribution of spike durations as defined by peak-to-trough time, with three obvious peaks. Based on previous studies examining the detailed differences in spike waveform and spike train statistics 32–35 , the long and medium duration waveforms likely correspond predominantly to the spiking of putative excitatory neurons and inhibitory neurons respectively. While short duration waveforms (SDWs) are not often isolated, a recent study suggests that these might reflect afferent spiking activity 35 .We arbitrarily assigned parts of the distribution to these categories, acknowledging that there is likely considerable overlap between the groups with different spike durations.…”

“…Based on previous studies examining the detailed differences in spike waveform and spike train statistics 32–35 , the long and medium duration waveforms likely correspond predominantly to the spiking of putative excitatory neurons and inhibitory neurons respectively. While short duration waveforms (SDWs) are not often isolated, a recent study suggests that these might reflect afferent spiking activity 35 .We arbitrarily assigned parts of the distribution to these categories, acknowledging that there is likely considerable overlap between the groups with different spike durations. Nevertheless, in line with the literature, median spike rates were significantly higher in the putative inhibitory neuron group compared to both other groups (n inhibitory =589, n excitatory =490, n SDW =88, Wilcoxon rank sum, p inhibitory-excitatory =2.33×10 −4 , p inhibitory-SDW = 4.09×10 −11 ).…”

Chronic Inactivation of the Orbitofrontal Cortex Increases Anxiety-Like Behavior and Impulsive Aggression, but Decreases Depression-Like Behavior in Rats

“…Because they could cause unintended damage to other brain regions connected anterogradely or retrogradely (Vanburen, 1963; Poduri et al, 1995) and to passing fibers, respectively, the effect of the lesion and inactivation might not have been restricted to the OFC. On the other hand, in the present experiments, we have inactivated the OFC using muscimol, which selectively inhibits somatic action potentials and exerts fewer effects on axons because of the sparse density of axonal GABA A receptors (Martin and Ghez, 1999; Robbins et al, 2013). Therefore, the present results demonstrate that chronic inactivation restricted to the VO/LO can augment anxiety-like behavior in rats.…”