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Asymmetric multisensory interactions of visual and somatosensory responses in a region of the rat parietal cortex.

Lippert MT, Takagaki K, Kayser C, Ohl FW - PLoS ONE (2013)

Bottom Line: Perception greatly benefits from integrating multiple sensory cues into a unified percept.Surprisingly, a selective asymmetry was observed in multisensory interactions: when the somatosensory response preceded the visual response, supra-linear summation of CSD was observed, but the reverse stimulus order resulted in sub-linear effects in the CSD.Our results highlight the rodent parietal cortex as a system to model the neural underpinnings of multisensory processing in behaving animals and at the cellular level.

View Article: PubMed Central - PubMed

Affiliation: Department Systems Physiology of Learning, Leibniz Institute for Neurobiology, Magdeburg, Germany. mlippert@lin-magdeburg.de

ABSTRACT
Perception greatly benefits from integrating multiple sensory cues into a unified percept. To study the neural mechanisms of sensory integration, model systems are required that allow the simultaneous assessment of activity and the use of techniques to affect individual neural processes in behaving animals. While rodents qualify for these requirements, little is known about multisensory integration and areas involved for this purpose in the rodent. Using optical imaging combined with laminar electrophysiological recordings, the rat parietal cortex was identified as an area where visual and somatosensory inputs converge and interact. Our results reveal similar response patterns to visual and somatosensory stimuli at the level of current source density (CSD) responses and multi-unit responses within a strip in parietal cortex. Surprisingly, a selective asymmetry was observed in multisensory interactions: when the somatosensory response preceded the visual response, supra-linear summation of CSD was observed, but the reverse stimulus order resulted in sub-linear effects in the CSD. This asymmetry was not present in multi-unit activity however, which showed consistently sub-linear interactions. These interactions were restricted to a specific temporal window, and pharmacological tests revealed significant local intra-cortical contributions to this phenomenon. Our results highlight the rodent parietal cortex as a system to model the neural underpinnings of multisensory processing in behaving animals and at the cellular level.

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Related in: MedlinePlus

Functional localization of a multisensory parietal area.A: Intrinsic optical imaging was used to localize responses evoked by visual, somatosensory and simultaneous bimodal stimuli. Color maps show activation from a typical session, 1 s after the stimulus. Anatomical areas are delineated in white according to Paxinos and Watson [73]. B: Schematic of sensory areas (as in A) together with locations of individual recording sites in parietal (white stars) and visual (yellow circles) cortices. Small insert: localization of the area on the rat brain. C: Left panel: Region of overlapping activation by unisensory stimuli. White region indicates overlap areas with median correlation to both unisensory stimuli. Right panel: Dual-color overlay of visual and somatosensory responses. Intermediate (violet) colors indicate activation by both stimuli. The white cross indicates the multisensory recording location chosen for subsequent electrophysiology. D: Comparison of measured mean hemodynamic signal (blue, mean response) and artificial gamma-function based hemodynamic response (orange, gamma) used for correlation analysis in panel C. The artificial hemodynamic response was constructed from the stimulus pulse train convolved with a gamma probability density function and closely resembles the measured signal time course. E: Fluorescence micrograph of recording location marked by fluorescent dye DiI. The cortical mantle is delineated by the dashed white markings. The right panel shows how the red fluorescence dye has stained the tissue around the electrode trace in the center of the image. Damage from the electrode was minimal. F: Example histological slice from the multisensory parietal region together with a schematic overlay of the multichannel electrode used for recording. Note the morphological characteristics of the association-type cortex with compact layer II and a virtual absence of layer IV. G: Current source density (CSD) analysis of example data (event-related potentials), with current sinks indicated by bright colors (dark areas are equalizing current sources). The strongest activation is located at the depth of the first granular sink (GS, see Results), and an additional sink, likely reflecting direct thalamic input, in layer IV can be seen (*). An infra-granular current sink (IS) and a later supra-granular sink are also visible (SS, falls outside the time window shown for the visual response). The average MUA response (black trace) is overlaid on the CSD data, and shows that both visual and somatosensory stimuli are effective in driving local multi-unit firing. H: Stimulus-response curve from one electrophysiology experiment. The ordinate shows the normalized response amplitude (AVREC) for the probed stimulation intensities denoted on the abscissa. The green rectangle covers the range from which stimuli could be chosen (50 to 90%). The arrow indicates the intensity used in this animal for the main experiments. V1: primary visual cortex, V2: secondary visual cortex, SC: somatosensory cortex, bf: barrel sub-field, PtA: parietal association area, AC: auditory cortex.
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pone-0063631-g001: Functional localization of a multisensory parietal area.A: Intrinsic optical imaging was used to localize responses evoked by visual, somatosensory and simultaneous bimodal stimuli. Color maps show activation from a typical session, 1 s after the stimulus. Anatomical areas are delineated in white according to Paxinos and Watson [73]. B: Schematic of sensory areas (as in A) together with locations of individual recording sites in parietal (white stars) and visual (yellow circles) cortices. Small insert: localization of the area on the rat brain. C: Left panel: Region of overlapping activation by unisensory stimuli. White region indicates overlap areas with median correlation to both unisensory stimuli. Right panel: Dual-color overlay of visual and somatosensory responses. Intermediate (violet) colors indicate activation by both stimuli. The white cross indicates the multisensory recording location chosen for subsequent electrophysiology. D: Comparison of measured mean hemodynamic signal (blue, mean response) and artificial gamma-function based hemodynamic response (orange, gamma) used for correlation analysis in panel C. The artificial hemodynamic response was constructed from the stimulus pulse train convolved with a gamma probability density function and closely resembles the measured signal time course. E: Fluorescence micrograph of recording location marked by fluorescent dye DiI. The cortical mantle is delineated by the dashed white markings. The right panel shows how the red fluorescence dye has stained the tissue around the electrode trace in the center of the image. Damage from the electrode was minimal. F: Example histological slice from the multisensory parietal region together with a schematic overlay of the multichannel electrode used for recording. Note the morphological characteristics of the association-type cortex with compact layer II and a virtual absence of layer IV. G: Current source density (CSD) analysis of example data (event-related potentials), with current sinks indicated by bright colors (dark areas are equalizing current sources). The strongest activation is located at the depth of the first granular sink (GS, see Results), and an additional sink, likely reflecting direct thalamic input, in layer IV can be seen (*). An infra-granular current sink (IS) and a later supra-granular sink are also visible (SS, falls outside the time window shown for the visual response). The average MUA response (black trace) is overlaid on the CSD data, and shows that both visual and somatosensory stimuli are effective in driving local multi-unit firing. H: Stimulus-response curve from one electrophysiology experiment. The ordinate shows the normalized response amplitude (AVREC) for the probed stimulation intensities denoted on the abscissa. The green rectangle covers the range from which stimuli could be chosen (50 to 90%). The arrow indicates the intensity used in this animal for the main experiments. V1: primary visual cortex, V2: secondary visual cortex, SC: somatosensory cortex, bf: barrel sub-field, PtA: parietal association area, AC: auditory cortex.

Mentions: For optical imaging, the skull was exposed and thinned over visual and somatosensory areas of the left hemisphere. Thinned skull is sufficiently transparent to record intrinsic optical signals, while also maintaining mechanical stability of the cortical surface, reducing movement artifacts and minimizing cortical damage and edema. A drop of silicone oil (60.000 cSt, Dow Corning Corporation) was applied to reduce glare. The animal was positioned on a vibration isolation table (Minus K Technology) under a macroscope [57], which projected a field of view approximately 7 mm in diameter onto a high-speed CCD camera (Jai TM-6740 GE, Stemmer-Imaging). Homogeneous dark field epi-illumination was provided by a custom-made ring illumination with high-intensity green LEDs (530 nm). Green light was chosen to measure the blood volume signal as suggested by a recent report [58]. The larger magnitude of this signal compared to red light signal further reduces artifacts (note the virtual absence of blood vessel artifacts in Fig. 1A) and minimizes time spent during optical recording. Also note the rapid onset of the signal (Fig. 1D), comparable to the timescale of red light signals. The entire setup was located in a sound-attenuated chamber. Data from the CCD camera was captured with an ActiveX plug-in (ActiveGigE, A&B Software LLC) from Matlab (The MathWorks Inc.) at a resolution of 640×480 pixels and 180-Hz frame rate.


Asymmetric multisensory interactions of visual and somatosensory responses in a region of the rat parietal cortex.

Lippert MT, Takagaki K, Kayser C, Ohl FW - PLoS ONE (2013)

Functional localization of a multisensory parietal area.A: Intrinsic optical imaging was used to localize responses evoked by visual, somatosensory and simultaneous bimodal stimuli. Color maps show activation from a typical session, 1 s after the stimulus. Anatomical areas are delineated in white according to Paxinos and Watson [73]. B: Schematic of sensory areas (as in A) together with locations of individual recording sites in parietal (white stars) and visual (yellow circles) cortices. Small insert: localization of the area on the rat brain. C: Left panel: Region of overlapping activation by unisensory stimuli. White region indicates overlap areas with median correlation to both unisensory stimuli. Right panel: Dual-color overlay of visual and somatosensory responses. Intermediate (violet) colors indicate activation by both stimuli. The white cross indicates the multisensory recording location chosen for subsequent electrophysiology. D: Comparison of measured mean hemodynamic signal (blue, mean response) and artificial gamma-function based hemodynamic response (orange, gamma) used for correlation analysis in panel C. The artificial hemodynamic response was constructed from the stimulus pulse train convolved with a gamma probability density function and closely resembles the measured signal time course. E: Fluorescence micrograph of recording location marked by fluorescent dye DiI. The cortical mantle is delineated by the dashed white markings. The right panel shows how the red fluorescence dye has stained the tissue around the electrode trace in the center of the image. Damage from the electrode was minimal. F: Example histological slice from the multisensory parietal region together with a schematic overlay of the multichannel electrode used for recording. Note the morphological characteristics of the association-type cortex with compact layer II and a virtual absence of layer IV. G: Current source density (CSD) analysis of example data (event-related potentials), with current sinks indicated by bright colors (dark areas are equalizing current sources). The strongest activation is located at the depth of the first granular sink (GS, see Results), and an additional sink, likely reflecting direct thalamic input, in layer IV can be seen (*). An infra-granular current sink (IS) and a later supra-granular sink are also visible (SS, falls outside the time window shown for the visual response). The average MUA response (black trace) is overlaid on the CSD data, and shows that both visual and somatosensory stimuli are effective in driving local multi-unit firing. H: Stimulus-response curve from one electrophysiology experiment. The ordinate shows the normalized response amplitude (AVREC) for the probed stimulation intensities denoted on the abscissa. The green rectangle covers the range from which stimuli could be chosen (50 to 90%). The arrow indicates the intensity used in this animal for the main experiments. V1: primary visual cortex, V2: secondary visual cortex, SC: somatosensory cortex, bf: barrel sub-field, PtA: parietal association area, AC: auditory cortex.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3646793&req=5

pone-0063631-g001: Functional localization of a multisensory parietal area.A: Intrinsic optical imaging was used to localize responses evoked by visual, somatosensory and simultaneous bimodal stimuli. Color maps show activation from a typical session, 1 s after the stimulus. Anatomical areas are delineated in white according to Paxinos and Watson [73]. B: Schematic of sensory areas (as in A) together with locations of individual recording sites in parietal (white stars) and visual (yellow circles) cortices. Small insert: localization of the area on the rat brain. C: Left panel: Region of overlapping activation by unisensory stimuli. White region indicates overlap areas with median correlation to both unisensory stimuli. Right panel: Dual-color overlay of visual and somatosensory responses. Intermediate (violet) colors indicate activation by both stimuli. The white cross indicates the multisensory recording location chosen for subsequent electrophysiology. D: Comparison of measured mean hemodynamic signal (blue, mean response) and artificial gamma-function based hemodynamic response (orange, gamma) used for correlation analysis in panel C. The artificial hemodynamic response was constructed from the stimulus pulse train convolved with a gamma probability density function and closely resembles the measured signal time course. E: Fluorescence micrograph of recording location marked by fluorescent dye DiI. The cortical mantle is delineated by the dashed white markings. The right panel shows how the red fluorescence dye has stained the tissue around the electrode trace in the center of the image. Damage from the electrode was minimal. F: Example histological slice from the multisensory parietal region together with a schematic overlay of the multichannel electrode used for recording. Note the morphological characteristics of the association-type cortex with compact layer II and a virtual absence of layer IV. G: Current source density (CSD) analysis of example data (event-related potentials), with current sinks indicated by bright colors (dark areas are equalizing current sources). The strongest activation is located at the depth of the first granular sink (GS, see Results), and an additional sink, likely reflecting direct thalamic input, in layer IV can be seen (*). An infra-granular current sink (IS) and a later supra-granular sink are also visible (SS, falls outside the time window shown for the visual response). The average MUA response (black trace) is overlaid on the CSD data, and shows that both visual and somatosensory stimuli are effective in driving local multi-unit firing. H: Stimulus-response curve from one electrophysiology experiment. The ordinate shows the normalized response amplitude (AVREC) for the probed stimulation intensities denoted on the abscissa. The green rectangle covers the range from which stimuli could be chosen (50 to 90%). The arrow indicates the intensity used in this animal for the main experiments. V1: primary visual cortex, V2: secondary visual cortex, SC: somatosensory cortex, bf: barrel sub-field, PtA: parietal association area, AC: auditory cortex.
Mentions: For optical imaging, the skull was exposed and thinned over visual and somatosensory areas of the left hemisphere. Thinned skull is sufficiently transparent to record intrinsic optical signals, while also maintaining mechanical stability of the cortical surface, reducing movement artifacts and minimizing cortical damage and edema. A drop of silicone oil (60.000 cSt, Dow Corning Corporation) was applied to reduce glare. The animal was positioned on a vibration isolation table (Minus K Technology) under a macroscope [57], which projected a field of view approximately 7 mm in diameter onto a high-speed CCD camera (Jai TM-6740 GE, Stemmer-Imaging). Homogeneous dark field epi-illumination was provided by a custom-made ring illumination with high-intensity green LEDs (530 nm). Green light was chosen to measure the blood volume signal as suggested by a recent report [58]. The larger magnitude of this signal compared to red light signal further reduces artifacts (note the virtual absence of blood vessel artifacts in Fig. 1A) and minimizes time spent during optical recording. Also note the rapid onset of the signal (Fig. 1D), comparable to the timescale of red light signals. The entire setup was located in a sound-attenuated chamber. Data from the CCD camera was captured with an ActiveX plug-in (ActiveGigE, A&B Software LLC) from Matlab (The MathWorks Inc.) at a resolution of 640×480 pixels and 180-Hz frame rate.

Bottom Line: Perception greatly benefits from integrating multiple sensory cues into a unified percept.Surprisingly, a selective asymmetry was observed in multisensory interactions: when the somatosensory response preceded the visual response, supra-linear summation of CSD was observed, but the reverse stimulus order resulted in sub-linear effects in the CSD.Our results highlight the rodent parietal cortex as a system to model the neural underpinnings of multisensory processing in behaving animals and at the cellular level.

View Article: PubMed Central - PubMed

Affiliation: Department Systems Physiology of Learning, Leibniz Institute for Neurobiology, Magdeburg, Germany. mlippert@lin-magdeburg.de

ABSTRACT
Perception greatly benefits from integrating multiple sensory cues into a unified percept. To study the neural mechanisms of sensory integration, model systems are required that allow the simultaneous assessment of activity and the use of techniques to affect individual neural processes in behaving animals. While rodents qualify for these requirements, little is known about multisensory integration and areas involved for this purpose in the rodent. Using optical imaging combined with laminar electrophysiological recordings, the rat parietal cortex was identified as an area where visual and somatosensory inputs converge and interact. Our results reveal similar response patterns to visual and somatosensory stimuli at the level of current source density (CSD) responses and multi-unit responses within a strip in parietal cortex. Surprisingly, a selective asymmetry was observed in multisensory interactions: when the somatosensory response preceded the visual response, supra-linear summation of CSD was observed, but the reverse stimulus order resulted in sub-linear effects in the CSD. This asymmetry was not present in multi-unit activity however, which showed consistently sub-linear interactions. These interactions were restricted to a specific temporal window, and pharmacological tests revealed significant local intra-cortical contributions to this phenomenon. Our results highlight the rodent parietal cortex as a system to model the neural underpinnings of multisensory processing in behaving animals and at the cellular level.

Show MeSH
Related in: MedlinePlus