Functional anatomy of the inferior colliculus and the auditory cortex: current source density analyses of click-evoked potentials

doi:10.1016/0378-5955(84)90003-0

Hearing Research

Volume 16, Issue 2, November 1984, Pages 133-142

https://doi.org/10.1016/0378-5955(84)90003-0 Get rights and content

Abstract

1.
1. In the auditory midbrain (inferior colliculus) and cortex (superior temporal gyrus) of awake squirrel monkeys profiles of click-evoked field potentials were recorded. The recording tracks were reconstructed anatomically. From the field potentials the one-dimensional current source density (CSD) distributions were calculated.
2.
2. By comparing the CSD profiles with the anatomical features of the reconstructed recording paths, the components of the CSDs could be attributed to certain anatomical sites. Thus a physiological method for the functional identification of recording sites was obtained. It permits the identification of depth locations of specific laminae in cortex. In the inferior colliculus it permits distinction between central and peripheral regions and between three depth segments.
3.
3. The CSDs in the central nucleus of the inferior colliculus lend functional support to the anatomical division into three distinct parts and, in addition, provide the temporal aspects of the main groups of synaptic activities.
4.
4. The CSDs in the auditory cortex permit determination of five different groups of excitatory synaptic activations. The spatio-temporal distributions of these components are very similar to those obtained in other neocortical areas and thus corroborate the hypothesis that afferent activity is relayed very similarly in all sensory areas of neocortex. squirrel monkey, inferior colliculus, auditory cortex, click-evoked potential. CSD distribution, functional anatomy

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Evoked neural responses to sensory stimuli have been extensively investigated in humans and animal models both to enhance our understanding of brain function and to aid in clinical diagnosis of neurological and neuropsychiatric conditions. Recording and imaging techniques such as electroencephalography (EEG), magnetoencephalography (MEG), local field potentials (LFPs), and calcium imaging provide complementary information about different aspects of brain activity at different spatial and temporal scales. Modeling and simulations provide a way to integrate these different types of information to clarify underlying neural mechanisms.
In this study, we aimed to shed light on the neural dynamics underlying auditory evoked responses by fitting a rate-based model to LFPs recorded via multi-contact electrodes which simultaneously sampled neural activity across cortical laminae. Recordings included neural population responses to best-frequency (BF) and non-BF tones at four representative sites in primary auditory cortex (A1) of awake monkeys. The model considered major neural populations of excitatory, parvalbumin-expressing (PV), and somatostatin-expressing (SOM) neurons across layers 2/3, 4, and 5/6. Unknown parameters, including the connection strength between the populations, were fitted to the data. Our results revealed similar population dynamics, fitted model parameters, predicted equivalent current dipoles (ECD), tuning curves, and lateral inhibition profiles across recording sites and animals, in spite of quite different extracellular current distributions. We found that PV firing rates were higher in BF than in non-BF responses, mainly due to different strengths of tonotopic thalamic input, whereas SOM firing rates were higher in non-BF than in BF responses due to lateral inhibition.
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Citation Excerpt :
The electrode depth was verified by small positive deflections and larger negative deflections of LFPs in the superficial cortex and deeper sites, respectively (Kaur et al., 2005). To determine the location of each electrode site within the cortical layers, we also performed a CSD analysis (Müller-Preuss and Mitzdorf, 1984; Kaur et al. 2005) after averaging the LFPs between neighboring electrodes (see the next section). The cortical depth with a clear source-sink-source pattern was detected to putatively determine layer 4 (Kaur et al., 2005; Sakata and Harris, 2009; Osanai and Tateno, 2016), consistent with previous anatomical investigations of cortical layer thickness (DeFelipe et al., 2002).
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Corticothalamic (CT) neurons comprise the largest component of the descending sensory corticofugal pathway, but their contributions to brain function and behavior remain an unsolved mystery. To address the hypothesis that layer 6 (L6) CTs may be activated by extra-sensory inputs prior to anticipated sounds, we performed optogenetically targeted single-unit recordings and two-photon imaging of Ntsr1-Cre+ L6 CT neurons in the primary auditory cortex (A1) while mice were engaged in an active listening task. We found that L6 CTs and other L6 units began spiking hundreds of milliseconds prior to orofacial movements linked to sound presentation and reward, but not to other movements such as locomotion, which were not linked to an explicit behavioral task. Rabies tracing of monosynaptic inputs to A1 L6 CT neurons revealed a narrow strip of cholinergic and non-cholinergic projection neurons in the external globus pallidus, suggesting a potential source of motor-related input. These findings identify new pathways and local circuits for motor modulation of sound processing and suggest a new role for CT neurons in active sensing.
Micro-coil-induced Inhomogeneous Electric Field Produces sound-driven-like Neural Responses in Microcircuits of the Mouse Auditory Cortex In Vivo
2018, Neuroscience
Citation Excerpt :
The electrode depth was verified by small positive deflections and larger negative deflections of the LFP in the superficial cortex and the deeper sites, respectively (Kaur et al., 2005). To identify cortical layers, we also performed a current-source density (CSD) analysis by calculating the second spatial derivative of the average LFP along the electrode sites (Muller-Preuss and Mitzdorf, 1984; Kaur et al., 2005), after averaging the LFPs between neighboring electrodes. The cortical depth with a clear source-sink-source pattern was detected to determine putative layer 4 (Kaur et al., 2005; Sakata and Harris, 2009; Osanai and Tateno, 2016b), which was consistent with the anatomical investigation of the cortical layer thickness (DeFelipe et al., 2002).
Magnetic stimulation is widely used in neuroscience research and clinical treatment. Despite recent progress in understanding the neural modulation mechanism of conventional magnetic stimulation methods, the physiological mechanism at the cortical microcircuit level is not well understood due to the poor stimulation focality and large electric artifact in the recording. To overcome these issues, we used a sub-millimeter-sized coil (micro-coil) to stimulate the mouse auditory cortex in vivo. To determine the mechanism, we conducted the first direct electrophysiological recording of micro-coil-driven neural responses at multiple sites on the horizontal surface and laminar areas of the auditory cortex. The laminar responses of local field potentials (LFPs) to the magnetic stimulation reached layer 6, and the spatiotemporal profiles were very similar to those of the acoustic stimulation, suggesting the activation of the same cortical microcircuit. The horizontal LFP responses to the magnetic stimulation were evoked within a millimeter-wide area around the stimulation coil. The activated cortical area was dependent on the coil orientation, providing useful information on the effective position of the coil relative to the brain surface for modulating cortical circuitry activity. In addition, numerical calculation of the induced electric field in the brain revealed that the inhomogeneity of the horizontal electric field to the surface is critical for micro-coil-induced cortical activation. The results suggest that our micro-coil technique has the potential to be used as a chronic, less-invasive and highly focal neuro-stimulator, and is useful for investigating microcircuit responses to magnetic stimulation for clinical treatment.
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Hearing Research

Abstract

References (20)

On the current that flows during the strychnine spike

Electroenceph. Clin. Neurophysiol.

A stereotaxic atlas of the brain of the squirrel monkey (Saimiri sciureus)

Cellular architecture and topographic organization of the inferior colliculus of the squirrel monkey

J. Comp. Neurol.

Some relations between resistivity and electrical activity in the cerebral cortex of the cat

J. Cell. Physiol. Suppl.

Analysis of field potentials in the central nervous system

A Study of Nerve Physiology, Chap. XVI

Cerebral representation of penile erection

J. Neurophysiol.

The current source density method and its application in the cat's cerebral cortex: investigation of evoked potentials and EEG phenomena

Physiol. Rev.

Visually evoked field potentials and current source densities in the cat visual cortex

J. Neurophysiol.

Cited by (83)

Changes in neural readout of response magnitude during auditory streaming do not correlate with behavioral choice in the auditory cortex

Laminar neural dynamics of auditory evoked responses: Computational modeling of local field potentials in auditory cortex of non-human primates

Temporal and spatial profiles of evoked activity induced by magnetic stimulation using millimeter-sized coils in the mouse auditory cortex in vivo

Auditory Corticothalamic Neurons Are Recruited by Motor Preparatory Inputs

Micro-coil-induced Inhomogeneous Electric Field Produces sound-driven-like Neural Responses in Microcircuits of the Mouse Auditory Cortex In Vivo

A Corticothalamic Circuit for Dynamic Switching between Feature Detection and Discrimination