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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 This Accepted Manuscript has not been copyedited and formatted. The final version may differ from this version. Research Articles: Behavioral/Cognitive Primary generators of visually evoked field potentials recorded in the macaque auditory cortex Yoshinao Kajikawa1,2, John F. Smiley3 and Charles E. Schroeder1,2 1Translational Neuroscience Division, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY 10962 2Cognitive Science and Neuromodulation Program, Dept. Neurosurgery, Columbia University, New York, NY 10032 3Department of Neurochemistry, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY 10962 DOI: 10.1523/JNEUROSCI.3800-16.2017 Received: 12 December 2016 Revised: 21 July 2017 Accepted: 25 July 2017 Published: 18 September 2017 Author contributions: Y.K. and C.E.S. designed research; Y.K. performed research; Y.K. contributed unpublished reagents/analytic tools; Y.K. and J.F.S. analyzed data; Y.K., J.F.S., and C.E.S. wrote the paper. Conflict of Interest: The authors declare no competing financial interests. We thank Dr. M. Klinger for veterinary assistance and Dr. D. Ross for technical support. This study was supported by NIH grants R01DC015780 and R01DC011490. Corresponding author: Yoshinao Kajikawa, Nathan Kline Institute, 140 Old Orangeburg Rd, Orangeburg, NY 10962, Email: [email protected], Phone: (845) 398-6630 Cite as: J. Neurosci ; 10.1523/JNEUROSCI.3800-16.2017 Alerts: Sign up at www.jneurosci.org/cgi/alerts to receive customized email alerts when the fully formatted version of this article is published. Accepted manuscripts are peer-reviewed but have not been through the copyediting, formatting, or proofreading process. Copyright © 2017 the authors ϭ Title: Ϯ Primary generators of visually evoked field potentials recorded in the macaque ϯ auditory cortex ϰ ϱ Abbreviated title: ϲ Face responses in the macaque auditory cortex ϳ ϴ Author names and affiliation, including postal codes: ϵ Yoshinao Kajikawa1,2, John F. Smiley3, Charles E. Schroeder1,2 ϭϬ 1. Translational Neuroscience Division, Nathan S. Kline Institute for Psychiatric ϭϭ Research, Orangeburg, NY 10962 ϭϮ 2. Cognitive Science and Neuromodulation Program, Dept. Neurosurgery, Columbia ϭϯ University, New York, NY 10032 ϭϰ 3. Department of Neurochemistry, Nathan S. Kline Institute for Psychiatric Research, ϭϱ Orangeburg, NY 10962 ϭϲ ϭϳ Corresponding author: ϭϴ Yoshinao Kajikawa ϭϵ Nathan Kline Institute ϮϬ 140 Old Orangeburg Rd, Orangeburg, NY 10962 Ϯϭ Email: [email protected] ϮϮ Phone: (845) 398-6630 Ϯϯ Ϯϰ Number of pages: 45 Ϯϱ Number of figures: 11 Ϯϲ Number of tables: 0 Ϯϳ Number of multimedia: 0 Ϯϴ Number of 3D models: 0 Ϯϵ ϯϬ Number of words, ϯϭ Abstract: 250 ϯϮ Introduction: 507 ϯϯ Discussion: 1441 ϯϰ ϯϱ Conflict of Interest: ϯϲ Authors declare no conflict of interests. ϯϳ ϯϴ Acknowledgements: ϯϵ We thank Dr. M. Klinger for veterinary assistance and Dr. D. Ross for technical support. ϰϬ This study was supported by NIH grants R01DC015780 and R01DC011490. ϰϭ ϰϮ ϭ ϰϯ ABSTRACT ϰϰ ϰϱ 3ULRUVWXGLHVKDYHUHSRUWHG³ORFDO´ILHOGSRWHQWLDO /)3 UHVSRQVHVWRIDFHVLQWKHPDFDTXH ϰϲ auditory cortex and have suggested that such face-LFPs may be substrates of audiovisual ϰϳ integration. However, while field potentials (FPs) may reflect the synaptic currents of ϰϴ neurons near the recording electrode, due to the use of a distant reference electrode, they ϰϵ often reflect those of synaptic activity occurring in distant sites as well. Thus, FP recordings ϱϬ within a given brain region (e.g., auditory cortex) may EH³FRQWDPLQDWHG´E\DFWLYLW\ ϱϭ generated elsewhere in the brain. To determine if face responses are in fact generated ϱϮ within macaque auditory cortex, we recorded FPs and concomitant multiunit activity (MUA) ϱϯ with linear array multielectrodes across auditory cortex in three macaques (one female), ϱϰ and applied current source density (CSD) analysis to the laminar FP profile. CSD analysis ϱϱ revealed no appreciable local generator contribution to the visual FP in auditory cortex, ϱϲ though we did note an increase in the amplitude of visual FP with cortical depth, suggesting ϱϳ that their generators are located below auditory cortex. In the underlying inferotemporal ϱϴ cortex we found polarity inversions of the main visual FP components accompanied by ϱϵ robust CSD responses and large amplitude MUA. These results indicate that face-evoked ϲϬ FP responses in auditory cortex are not generated locally, but are volume conducted from ϲϭ other face-responsive regions. In broader terms, our results underscore the caution that ϲϮ unless far-field contamination is removed, LFPs in general may UHIOHFWVXFK³IDUILHOG´ ϲϯ activity, in addition to or in absence of local synaptic responses. ϲϰ ϲϱ SIGNIFICANCE STATEMENT Ϯ ϲϲ ϲϳ Field potentials (FPs) can index neuronal population activity that is not evident in action ϲϴ potentials. However, due to volume conduction, field potentials may reflect activity in distant ϲϵ neurons superimposed upon that of neurons close to the recording electrode. This is ϳϬ problematic as the default assumption is that FPs originate from local activity, and thus are ϳϭ termed ³local´ (LFP). We examine this general problem in the context of previously reported ϳϮ face-evoked FPs in macaque auditory cortex. Our findings suggest that face-FPs are in fact ϳϯ generated in the underlying inferotemporal cortex and volume conducted to the auditory ϳϰ cortex. The note of caution raised by these findings is of particular importance for studies ϳϱ that seek to assign FP/LFP recordings to specific cortical layers. ϳϲ ϳϳ INTRODUCTION ϳϴ ϳϵ Field potentials (FPs) reflect neuronal ensemble activity (Schroeder et al., 1998; Buzsaki et ϴϬ al., 2012; Kajikawa and Schroeder, 2011), and often this activity is subthreshold to, or ϴϭ otherwise not evident in action potentials. In a large, primarily Ohmic medium like the brain, ϴϮ FPs can be approximated by a spatial integration of synaptically-mediated transmembrane ϴϯ currents that are weighted by their spatial proximity to a measuring point (Kajikawa and ϴϰ Schroeder, 2015). Ordinarily this would mean that, activity of neurons near the recording ϴϱ electrode (near field) is better represented in the FP than that of distant neurons. However ϴϲ remote (far field) activity can also influence FP, especially when it is stronger than local ϴϳ activity. When there are multiple neuronal populations that differ in their temporal activity ϯ ϴϴ patterns, FPs at sites in between exhibit temporal patterns that are mixtures of ϴϵ contributions from in those populations (Kajikawa and Schroeder, 2015). ϵϬ Visual activation/modulation of low level auditory cortex is considered to be an early ϵϭ stage substrate of audiovisual (AV) integration (Driver and Noesselt, 2008; Ghazanfar and ϵϮ Schroeder, 2006), and in macaques, it has been shown by several techniques measuring ϵϯ cortical activity: single/multiunit activity, local field potential (LFP) and functional imaging. ϵϰ Studies report no significant change in neuronal firing rate after visual stimuli, but rather, ϵϱ speeding of auditory response onsets (Chandrasekaran et al. 2013), and/or increase in the ϵϲ information carried by auditory-evoked firing patterns (Kayser et al., 2010). In contrast, ϵϳ visual stimuli, particularly faces, not only modulate auditory LFP responses (Ghazanfar et ϵϴ al., 2005), but also evoke LFPs by themselves (Hoffman et al., 2008; Kayser et al., 2007a, ϵϵ 2008). Visual-evoked LFPs with little to no change in local neuronal firing suggest that ϭϬϬ either (a) visual stimuli alone evoke sub-threshold synaptic responses, or (b) visual-evoked ϭϬϭ LFP reflect far field, rather than local activity. ϭϬϮ To better understand the nature of visual responses in auditory cortex, we recorded ϭϬϯ laminar profiles of FPs and concomitant multiunit activity (MUA) from auditory cortex in ϭϬϰ macaques performing auditory and visual tasks. Since previous studies argued that ϭϬϱ conspecific faces were the most effective modulators of responses to conspecific vocal ϭϬϲ sounds in auditory cortex (Ghazanfar et al., 2005; Hoffman et al., 2008), the present study ϭϬϳ focused on the responses to macaque monkey faces. FP recordings were augmented by ϭϬϴ current source density (CSD) analysis. Because it eliminates effects of volume conduction, ϭϬϵ CSD is a better indicator of local activity than FPs alone (Kajikawa and Schroeder, 2011). ϭϭϬ While FP responded strongly to faces, associated CSD and MUA responses were ϰ ϭϭϭ negligible, indicating little to no local contribution to generation of the face-evoked visual FP ϭϭϮ response. Instead, visual FP responses grew larger with depth within and below auditory ϭϭϯ cortex. Tracking the FP responses below auditory cortex revealed visual MUA and CSD ϭϭϰ responses in the inferotemporal (IT) cortex. Our results indicate that face-evoked FP ϭϭϱ responses in auditory cortex are primarily far field reflections of responses generated in IT. ϭϭϲ Thus, while FP methods clearly provide unique and valuable information on population ϭϭϳ neuronal activity, strict localization of their sources requires spatial differentiation over 2 or ϭϭϴ more recordings at millimeter/sub-millimeter scales. ϭϭϵ ϭϮϬ MATERIALS AND METHODS ϭϮϭ ϭϮϮ All procedures were approved by the IACUC of the Nathan Kline Institute. ϭϮϯ ϭϮϰ Subjects ϭϮϱ Three macaque monkeys (Macaca mulatta; P: female, G and W: males) were implanted ϭϮϲ with headposts and recording chambers (one per hemisphere, both sides in P and right ϭϮϳ side in G and W) using aseptic surgical techniques. Based on presurgical MRI, the ϭϮϴ chambers were positioned to aim penetrations perpendicular to auditory cortices on the ϭϮϵ lower bank of the lateral sulcus. ϭϯϬ ϭϯϭ Behavioral paradigms ϭϯϮ Monkeys were trained to perform the auditory and visual oddball tasks in a sound- ϭϯϯ attenuated chamber. The monkey started a trial by pulling a lever that brought up a gray ϱ ϭϯϰ rectangle area (17.8 x 11.4 degrees) on the screen (Fig. 1A). The monkey then maintained ϭϯϱ gaze position within the window for at least 400 ms to initiate a sequence of sensory events ϭϯϲ that started with a static image appearing in the window for 900 ms, followed by a 500 ms ϭϯϳ non-target stimulus.
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