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Primary Generators of Visually Evoked Field Potentials Recorded in the Macaque Auditory Cortex

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Primary Generators of Visually Evoked Field Potentials Recorded in the Macaque Auditory Cortex The Journal of Neuroscience, October 18, 2017 • 37(42):10139–10153 • 10139 Behavioral/Cognitive Primary Generators of Visually Evoked Field Potentials Recorded in the Macaque Auditory Cortex Yoshinao Kajikawa,1,2 John F. Smiley,3 and Charles E. Schroeder1,2 1Translational Neuroscience Division, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, New York 10962, 2Cognitive Science and Neuromodulation Program, Department Neurosurgery, Columbia University, New York, New York 10032, and 3Department of Neurochemistry, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, New York 10962 Prior studies have reported “local” field potential (LFP) responses to faces in the macaque auditory cortex and have suggested that such face-LFPs may be substrates of audiovisual integration. However, although field potentials (FPs) may reflect the synaptic currents of neurons near the recording electrode, due to the use of a distant reference electrode, they often reflect those of synaptic activity occurring in distant sites as well. Thus, FP recordings within a given brain region (e.g., auditory cortex) may be “contaminated” by activity generated elsewhere in the brain. To determine whether face responses are indeed generated within macaque auditory cortex, we recordedFPsandconcomitantmultiunitactivitywithlineararraymultielectrodesacrossauditorycortexinthreemacaques(onefemale), and applied current source density (CSD) analysis to the laminar FP profile. CSD analysis revealed no appreciable local generator contribution to the visual FP in auditory cortex, although we did note an increase in the amplitude of visual FP with cortical depth, suggesting that their generators are located below auditory cortex. In the underlying inferotemporal cortex, we found polarity inversions of the main visual FP components accompanied by robust CSD responses and large-amplitude multiunit activity. These results indicate that face-evoked FP responses in auditory cortex are not generated locally but are volume-conducted from other face-responsive regions. In broader terms, our results underscore the caution that, unless far-field contamination is removed, LFPs in general may reflect such “far-field” activity, in addition to, or in absence of, local synaptic responses. Key words: auditory cortex; face response; field potential; inferotemporal cortex; macaque monkey; volume conduction Significance Statement Field potentials (FPs) can index neuronal population activity that is not evident in action potentials. However, due to volume conduction, FPs may reflect activity in distant neurons superimposed upon that of neurons close to the recording electrode. This is problematic as the default assumption is that FPs originate from local activity, and thus are termed “local” (LFP). We examine this general problem in the context of previously reported face-evoked FPs in macaque auditory cortex. Our findings suggest that face-FPs are indeed generated in the underlying inferotemporal cortex and volume-conducted to the auditory cortex. The note of caution raised by these findings is of particular importance for studies that seek to assign FP/LFP recordings to specific cortical layers. Introduction evident in, action potentials (APs). In a large, primarily Ohmic Field potentials (FPs) reflect neuronal ensemble activity (Schroe- medium, such as the brain, FPs can be approximated by a spatial der et al., 1998; Kajikawa and Schroeder, 2011; Buzsa´ki et al., integration of synaptically mediated transmembrane currents 2012), and often this activity is subthreshold to, or otherwise not that are weighted by their spatial proximity to a measuring point (Kajikawa and Schroeder, 2015). Ordinarily, this would mean Received Dec. 12, 2016; revised July 21, 2017; accepted July 25, 2017. that, activity of neurons near the recording electrode (near field) Author contributions: Y.K. and C.E.S. designed research; Y.K. performed research; Y.K. contributed unpublished is better represented in the FP than that of distant neurons. How- reagents/analytic tools; Y.K. and J.F.S. analyzed data; Y.K., J.F.S., and C.E.S. wrote the paper. This study was supported by National Institutes of Health Grants R01DC015780 and R01DC011490. We thank ever, remote (far-field) activity can also influence FP, especially Dr. Mark Klinger for veterinary assistance; and Dr. Deborah Ross for technical support. when it is stronger than local activity. When there are multiple The authors declare no competing financial interests. neuronal populations that differ in their temporal activity pat- Correspondence should be addressed to Dr. Yoshinao Kajikawa, Nathan Kline Institute, 140 Old Orangeburg terns, FPs at sites in between exhibit temporal patterns that are Road, Orangeburg, NY 10962. E-mail: [email protected]. DOI:10.1523/JNEUROSCI.3800-16.2017 mixtures of contributions from in those populations (Kajikawa Copyright © 2017 the authors 0270-6474/17/3710139-15$15.00/0 and Schroeder, 2015). 10140 • J. Neurosci., October 18, 2017 • 37(42):10139–10153 Kajikawa et al. • Face Responses in the Macaque Auditory Cortex Visual activation/modulation of low level auditory cortex is onset of the following stimulus were randomly chosen from 600, 750, considered to be an early-stage substrate of audiovisual (AV) 900, 1050, and 1200 ms to reduce potential effects of cognitive entrain- integration (Ghazanfar and Schroeder, 2006; Driver and Noesselt, ment (Lakatos et al., 2009). Monkeys were required to maintain gaze 2008); and in macaques, it has been shown by several techniques position within a window until the target stimulus was presented regard- measuring cortical activity: single/multiunit activity (MUA), lo- less of the stimulus modality, and responded to the target manually by releasing the lever to obtain an aqueous reward. Every response was cal field potential (LFP), and functional imaging. Studies report followed by a Ͼ1 s blank period. Gaze position was monitored continu- no significant change in neuronal firing rate after visual stimuli, ously using Eyelink-1000 (SR-Research). Stimulus deliveries, tracking of but rather, speeding of auditory response onsets (Chandrasek- the lever, and reward deliveries were controlled using the Experiment aran et al., 2013), and/or increase in the information carried by Builder (SR-Research). auditory-evoked firing patterns (Kayser et al., 2010). In contrast, Stimuli. Movie clips of 9 exemplars of macaque vocalizations (courtesy visual stimuli, particularly faces, not only modulate auditory LFP of Prof. Romanski, University of Rochester, and others recorded at the responses (Ghazanfar et al., 2005), but also evoke LFPs by them- Nathan Kline Institute) were used. Clips were trimmed to start from selves (Kayser et al., 2007a, 2008; Hoffman et al., 2008). Visual- the onset of vocalizing face movements and to last for 500 ms using the evoked LFPs with little to no change in local neuronal firing Adobe Premiere (Adobe Systems), and separated into a visual track (15 suggest that either (1) visual stimuli alone evoke subthreshold frames, 29.97 fps) and an audio track (44.1 kHz sample rate) using the synaptic responses or (2) visual-evoked LFP reflect far-field, utility software of the Experiment Builder (SR-Research). Visual tracks were zoomed in using Adobe Premiere, so that faces occupied a central rather than local activity. zone of ϳ10 degrees diameter circle area when displayed on screen, and To better understand the nature of visual responses in audi- further edited to blacken the backgrounds behind the monkeys’ head and tory cortex, we recorded laminar profiles of FPs and concomitant below the collar using a custom script in MATLAB (The MathWorks). MUA from auditory cortex in macaques performing auditory For the AV trials, a movie track and an audio track were presented and visual tasks. Because previous studies argued that conspecific synchronously as nontarget and target stimuli. Sounds in the audio faces were the most effective modulators of responses to con- tracks started at 131–257 ms later than the onset of the visual tracks. In specific vocal sounds in auditory cortex (Ghazanfar et al., 2005; the following figures in Results, the timing of auditory stimuli and cor- Hoffman et al., 2008), the present study focused on the responses tical responses was shown with the same delayed timing as experiments. to macaque monkey faces. FP recordings were augmented by The visual-auditory offset is due to the delay from the initial visible current source density (CSD) analysis. Because it eliminates ef- articulation gesture to the onset of accompanying vocal sounds (Schroe- der et al., 2008; Chandrasekaran et al., 2011). For V-alone trials, a movie fects of volume conduction, CSD is a better indicator of local track was presented without audio track. For A-alone trials, an audio activity than FPs alone (Kajikawa and Schroeder, 2011). Whereas track was presented concurrently with a movie track of a static image (see FP responded strongly to faces, associated CSD and MUA re- below) that was shown from the period just before the stimulus. In effect, sponses were negligible, indicating little to no local contribution no noticeable change occurred in the image during the time the sounds to generation of the face-evoked visual FP response. Instead, vi- were played. The delayed onset timing of sound relative to the null- sual FP responses grew larger with depth within and below audi- motion movie track was the same as stimuli in AV trials. For both the AV tory cortex. Tracking
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