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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

Multisensory response patterns in parietal cortex.A: Example response time course of a granular layer CSD averaged across trials. The upper panel shows responses to each unimodal stimulus, with evoked somatosensory (gray) or visual (black) current sinks (negative values). The lower panel displays the response to the combined stimulus (solid) and the linearly predicted (lin. pred.) response, which is the arithmetic sum of the two unisensory responses (dashed). Here and in panels B, C, and D, the left column shows the responses for a stimulus onset asynchrony of 0 ms (physically synchronous stimuli), while the right panel displays responses for the visual stimulus preceding the somatosensory stimulus by an SOA of 50 ms. In both conditions, the response demonstrates a systematic deviation from the linear prediction, reflecting a non-linear multisensory interaction. For further analysis, we focused on the early part of this interaction (arrow and gray bar) and did not consider effects occurring much longer after stimulus offset (*).B: Distribution of measured and predicted (summed) multisensory CSD responses (strength of granular current sink) in individual experiments (gray dots). Responses to visual stimuli following a somatosensory response (SOA = 0 ms) are supra-linearly enhanced (left), while somatosensory responses following a visual stimulus (SOA = 50 ms) interact sub-linearly (right, the words ‘sub’ and ‘supra’ describe the interaction polarity on their side of the diagonal). More negative values indicate stronger current sinks. C: Example of sub-linear effect on multi-unit activity. The dashed line outlines the sum of unisensory responses, and the solid line represents the measured multisensory response. The gray bar indicates the 30 ms window used to capture the excitatory part of the response. Arrows denote the part of highest non-linearity. D: Distribution of measured and linearly predicted (summed) multisensory MUA responses. Regardless of stimulus onset asynchrony, a sub-linear interaction is observed. E: Multisensory enhancement index (MEI) for the granular CSD sink and MUA over a range of SOAs. CSD responses to visual stimuli preceded by a somatosensory response (black) show a supra-linear effect, while the reverse leads to a sub-linear effect (gray). Note that absolute SOA refers to the external physical SOA of the two stimuli, while relative SOA refers to the internal difference in response latency of the respective unimodal CSD responses. PS indicates the point of simultaneity (mean and s.d.) in individual experiments, at which activity onsets would coincide. Note that the curve is centered around the point of simultaneity and not around synchronous stimuli at an SOA of 0 ms. MUA (dashed line) shows a consistent sub-linear interaction, also restricted to a short time window around simultaneity.
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pone-0063631-g002: Multisensory response patterns in parietal cortex.A: Example response time course of a granular layer CSD averaged across trials. The upper panel shows responses to each unimodal stimulus, with evoked somatosensory (gray) or visual (black) current sinks (negative values). The lower panel displays the response to the combined stimulus (solid) and the linearly predicted (lin. pred.) response, which is the arithmetic sum of the two unisensory responses (dashed). Here and in panels B, C, and D, the left column shows the responses for a stimulus onset asynchrony of 0 ms (physically synchronous stimuli), while the right panel displays responses for the visual stimulus preceding the somatosensory stimulus by an SOA of 50 ms. In both conditions, the response demonstrates a systematic deviation from the linear prediction, reflecting a non-linear multisensory interaction. For further analysis, we focused on the early part of this interaction (arrow and gray bar) and did not consider effects occurring much longer after stimulus offset (*).B: Distribution of measured and predicted (summed) multisensory CSD responses (strength of granular current sink) in individual experiments (gray dots). Responses to visual stimuli following a somatosensory response (SOA = 0 ms) are supra-linearly enhanced (left), while somatosensory responses following a visual stimulus (SOA = 50 ms) interact sub-linearly (right, the words ‘sub’ and ‘supra’ describe the interaction polarity on their side of the diagonal). More negative values indicate stronger current sinks. C: Example of sub-linear effect on multi-unit activity. The dashed line outlines the sum of unisensory responses, and the solid line represents the measured multisensory response. The gray bar indicates the 30 ms window used to capture the excitatory part of the response. Arrows denote the part of highest non-linearity. D: Distribution of measured and linearly predicted (summed) multisensory MUA responses. Regardless of stimulus onset asynchrony, a sub-linear interaction is observed. E: Multisensory enhancement index (MEI) for the granular CSD sink and MUA over a range of SOAs. CSD responses to visual stimuli preceded by a somatosensory response (black) show a supra-linear effect, while the reverse leads to a sub-linear effect (gray). Note that absolute SOA refers to the external physical SOA of the two stimuli, while relative SOA refers to the internal difference in response latency of the respective unimodal CSD responses. PS indicates the point of simultaneity (mean and s.d.) in individual experiments, at which activity onsets would coincide. Note that the curve is centered around the point of simultaneity and not around synchronous stimuli at an SOA of 0 ms. MUA (dashed line) shows a consistent sub-linear interaction, also restricted to a short time window around simultaneity.

Mentions: MUA responses were obtained from high-pass filtered signals (0.9–8.8 kHz) as events passing a threshold determined manually for every channel during the experiment. The time course of MUA responses was binned at 5 ms resolution, and the average MUA during a 90 ms pre-stimulus window was subtracted to ensure equal baseline across channels and conditions. The amplitude of MUA responses was quantified in a window of 30 ms and for each experiment, responses were averaged over all channels that demonstrated a stimulus-related increase in firing. The window of 30 ms was chosen because it captured well the excitatory part of the MUA response (the window is depicted as grey bar in Figure 2C). If longer windows are used, the post-response hyperpolarization dependent suppression would be captured as well. Since these components are fundamentally different in nature, we chose to limit the analysis to this first part of the response. We used the same window for both modalities, since the transient excitatory segment of the MUA responses did not show such marked duration differences as seen in the CSD patterns.


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)

Multisensory response patterns in parietal cortex.A: Example response time course of a granular layer CSD averaged across trials. The upper panel shows responses to each unimodal stimulus, with evoked somatosensory (gray) or visual (black) current sinks (negative values). The lower panel displays the response to the combined stimulus (solid) and the linearly predicted (lin. pred.) response, which is the arithmetic sum of the two unisensory responses (dashed). Here and in panels B, C, and D, the left column shows the responses for a stimulus onset asynchrony of 0 ms (physically synchronous stimuli), while the right panel displays responses for the visual stimulus preceding the somatosensory stimulus by an SOA of 50 ms. In both conditions, the response demonstrates a systematic deviation from the linear prediction, reflecting a non-linear multisensory interaction. For further analysis, we focused on the early part of this interaction (arrow and gray bar) and did not consider effects occurring much longer after stimulus offset (*).B: Distribution of measured and predicted (summed) multisensory CSD responses (strength of granular current sink) in individual experiments (gray dots). Responses to visual stimuli following a somatosensory response (SOA = 0 ms) are supra-linearly enhanced (left), while somatosensory responses following a visual stimulus (SOA = 50 ms) interact sub-linearly (right, the words ‘sub’ and ‘supra’ describe the interaction polarity on their side of the diagonal). More negative values indicate stronger current sinks. C: Example of sub-linear effect on multi-unit activity. The dashed line outlines the sum of unisensory responses, and the solid line represents the measured multisensory response. The gray bar indicates the 30 ms window used to capture the excitatory part of the response. Arrows denote the part of highest non-linearity. D: Distribution of measured and linearly predicted (summed) multisensory MUA responses. Regardless of stimulus onset asynchrony, a sub-linear interaction is observed. E: Multisensory enhancement index (MEI) for the granular CSD sink and MUA over a range of SOAs. CSD responses to visual stimuli preceded by a somatosensory response (black) show a supra-linear effect, while the reverse leads to a sub-linear effect (gray). Note that absolute SOA refers to the external physical SOA of the two stimuli, while relative SOA refers to the internal difference in response latency of the respective unimodal CSD responses. PS indicates the point of simultaneity (mean and s.d.) in individual experiments, at which activity onsets would coincide. Note that the curve is centered around the point of simultaneity and not around synchronous stimuli at an SOA of 0 ms. MUA (dashed line) shows a consistent sub-linear interaction, also restricted to a short time window around simultaneity.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0063631-g002: Multisensory response patterns in parietal cortex.A: Example response time course of a granular layer CSD averaged across trials. The upper panel shows responses to each unimodal stimulus, with evoked somatosensory (gray) or visual (black) current sinks (negative values). The lower panel displays the response to the combined stimulus (solid) and the linearly predicted (lin. pred.) response, which is the arithmetic sum of the two unisensory responses (dashed). Here and in panels B, C, and D, the left column shows the responses for a stimulus onset asynchrony of 0 ms (physically synchronous stimuli), while the right panel displays responses for the visual stimulus preceding the somatosensory stimulus by an SOA of 50 ms. In both conditions, the response demonstrates a systematic deviation from the linear prediction, reflecting a non-linear multisensory interaction. For further analysis, we focused on the early part of this interaction (arrow and gray bar) and did not consider effects occurring much longer after stimulus offset (*).B: Distribution of measured and predicted (summed) multisensory CSD responses (strength of granular current sink) in individual experiments (gray dots). Responses to visual stimuli following a somatosensory response (SOA = 0 ms) are supra-linearly enhanced (left), while somatosensory responses following a visual stimulus (SOA = 50 ms) interact sub-linearly (right, the words ‘sub’ and ‘supra’ describe the interaction polarity on their side of the diagonal). More negative values indicate stronger current sinks. C: Example of sub-linear effect on multi-unit activity. The dashed line outlines the sum of unisensory responses, and the solid line represents the measured multisensory response. The gray bar indicates the 30 ms window used to capture the excitatory part of the response. Arrows denote the part of highest non-linearity. D: Distribution of measured and linearly predicted (summed) multisensory MUA responses. Regardless of stimulus onset asynchrony, a sub-linear interaction is observed. E: Multisensory enhancement index (MEI) for the granular CSD sink and MUA over a range of SOAs. CSD responses to visual stimuli preceded by a somatosensory response (black) show a supra-linear effect, while the reverse leads to a sub-linear effect (gray). Note that absolute SOA refers to the external physical SOA of the two stimuli, while relative SOA refers to the internal difference in response latency of the respective unimodal CSD responses. PS indicates the point of simultaneity (mean and s.d.) in individual experiments, at which activity onsets would coincide. Note that the curve is centered around the point of simultaneity and not around synchronous stimuli at an SOA of 0 ms. MUA (dashed line) shows a consistent sub-linear interaction, also restricted to a short time window around simultaneity.
Mentions: MUA responses were obtained from high-pass filtered signals (0.9–8.8 kHz) as events passing a threshold determined manually for every channel during the experiment. The time course of MUA responses was binned at 5 ms resolution, and the average MUA during a 90 ms pre-stimulus window was subtracted to ensure equal baseline across channels and conditions. The amplitude of MUA responses was quantified in a window of 30 ms and for each experiment, responses were averaged over all channels that demonstrated a stimulus-related increase in firing. The window of 30 ms was chosen because it captured well the excitatory part of the MUA response (the window is depicted as grey bar in Figure 2C). If longer windows are used, the post-response hyperpolarization dependent suppression would be captured as well. Since these components are fundamentally different in nature, we chose to limit the analysis to this first part of the response. We used the same window for both modalities, since the transient excitatory segment of the MUA responses did not show such marked duration differences as seen in the CSD patterns.

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