Three-dimensional localization of neurons in cortical tetrode recordings

Abstract

The recording radius and spatial selectivity of an extracellular probe are important for interpreting neurophysiological recordings but are rarely measured. Moreover, an analysis of the recording biophysics of multisite probes (e.g., tetrodes) can provide for source characterization and localization of spiking single units, but this capability has remained largely unexploited. Here we address both issues quantitatively. Advancing a tetrode (Ϸ40-m contact separation, tetrahedral geometry) in 5-to 10-m steps, we repeatedly recorded extracellular action potentials (EAPs) of single neurons in the visual cortex. Using measured spatial variation of EAPs, the tetrodes' measured geometry, and a volume conductor model of the cortical tissue, we solved the inverse problem of estimating the location and the size of the equivalent dipole model of the spike generator associated with each neuron. Half of the 61 visual neurons were localized within a radius of Ϸ100 m and 95% within Ϸ130 m around the tetrode tip (i.e., a large fraction was much further than previously thought). Because of the combined angular sensitivity of the tetrode's leads, location uncertainty was less than one-half the cell's distance. We quantified the spatial dependence of the probability of cell isolation, the isolated fraction, and the dependence of the recording radius on probe size and equivalent dipole size. We also reconstructed the spatial configuration of sets of simultaneously recorded neurons to demonstrate the potential use of 3D dipole localization for functional anatomy. Finally, we found that the dipole moment vector, surprisingly, tended to point toward the probe, leading to the interpretation that the equivalent dipole represents a "local lobe" of the dendritic arbor. recording radius; extracellular action potential; multisite recording; inverse problem; equivalent dipole; lead field theory MULTICONTACT RECORDINGS HAVE HIGH YIELD (Blanche et al. 2005;Csicsvari et al. 2003;Eckhorn and Thomas 1993;Gray et al. 1995;McNaughton et al. 1983) (Buzsaki and Kandel 1998;Drake et al. 1988;Henze et al. 2000) show, the shape and size of the extracellular action potential (EAP) waveform depends on the relative position of cell and probe. Thus, these recordings carry spatial information about spike sources that is not available in single electrode records. However, this spatial information is typically not exploited, because extracting it requires solution of an inverse problem, deducing the position and the size of the current source of a spiking neuron from measurements of its EAP at multiple locations.Here, we solve this inverse problem by modeling the spiking neuron with a single current dipole. The choice of a dipole model rests on reasoning presented in detail in a companion paper and its supplemental material (Mechler and Victor 2011). Briefly, although the membrane currents of a spiking neuron constitute a genuinely distributed current source, the resulting extracellular field is well approximated by that of a dipole beyond a minimum distance a...

Responses to Orientation Discontinuities in V1 and V2: Physiological Dissociations and Functional Implications

“…The preparation was similar to what was described previously (Mechler et al, 2002;Victor et al, 2006;Schmid et al, 2009) and is summarized here. After an overnight fast, animals were premedicated with atropine (0.05 mg/kg, i.m.…”

“…Only recording locations that we could unambiguously place within V1 or V2 were used for further analysis. Recording sites that were within ϳ250 m from the V1-V2 border were excluded because the tetrodes we used can pick up signals in a range of ϳ130 m (Mechler et al, 2011) and there is an additional uncertainty in localizing the center of the lesions and the reconstruction of recording sites between lesion.…”

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

“…Currently, tetrodes and silicon polytrodes using microelectromechanical systems (MEMS) technologies are the main tools of neuroscience laboratories performing extracellular electrophysiological experiments (Berényi et al 2014;Blanche et al 2005;Bragin et al 2000;Csicsvari et al 2003;Lopez et al 2014;Mechler et al 2011;Nguyen et al 2009;Seidl et al 2012). Despite the advantage of multiple recording sites, usually these devices need to be physically moved in the brain tissue after implantation to find the desired locations of neuronal activity.…”

The accuracy and precision of signal source localization with tetrodes

“…Several neuronal source localization algorithms have been proposed and used in vivo [3], [6], [7], [8], [9]. These methods employed various approaches ranging from simple heuristic EAP generative models [6], [7], to more biophysically realistic models, such as monopole [3], dipole [9], and line source [8] approximations.…”

“…These methods employed various approaches ranging from simple heuristic EAP generative models [6], [7], to more biophysically realistic models, such as monopole [3], dipole [9], and line source [8] approximations. However, since these experiments were performed in vivo where the exact location of neurons is unknown, the localization results could not be validated.…”