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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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Visual cortex shows less multisensory response.A: The total CSD response to both unimodal stimuli, expressed as averaged rectified CSD (AVREC), confirms the multisensory nature of the investigated parietal region and the near absence of somatosensory-evoked responses in visual cortex. B: CSD responses quantified as the deviation of the measured to the predicted linear multisensory response (SOA = 0 ms, vis&som – (vis+som)). Supra-linear interactions are marked by arrows in the granular (GS) and infra-granular sinks (IS) and also as a late effect in supra-granular layers (LE). Note the absence of multisensory response interactions in visual cortex (right panel, gray arrows mark the same locations as in left panel).
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pone-0063631-g003: Visual cortex shows less multisensory response.A: The total CSD response to both unimodal stimuli, expressed as averaged rectified CSD (AVREC), confirms the multisensory nature of the investigated parietal region and the near absence of somatosensory-evoked responses in visual cortex. B: CSD responses quantified as the deviation of the measured to the predicted linear multisensory response (SOA = 0 ms, vis&som – (vis+som)). Supra-linear interactions are marked by arrows in the granular (GS) and infra-granular sinks (IS) and also as a late effect in supra-granular layers (LE). Note the absence of multisensory response interactions in visual cortex (right panel, gray arrows mark the same locations as in left panel).

Mentions: When both stimuli were presented simultaneously (physical stimulus onset asynchrony = 0 ms) the CSD response to the combined stimulus consisted of a leading somatosensory-evoked sink followed by a later visual-evoked sink (Fig. 2A, left), as was expected given the differences in response latencies between the two modalities. Importantly, the somatosensory stimulus (whose activation emerges first) induces a supra-linear enhancement of the amplitude of the visual-evoked current sink; that is, the sink becomes stronger (more negative). This multisensory interaction can be seen in the comparison of the multisensory response and the prediction from the sum of unisensory responses (Fig. 2A, lower panels). The scaled magnitude of this difference is represented by the MEI. The difference between the multisensory response and the unisensory sum was significant across experiments (n = 10, multisensory enhancement index (MEI) = 21.6±4%, mean±s.e.m, Wilcoxon signed rank test: P<0.01, Fig. 2B). A similar effect was seen in the infra-granular sink, albeit to a lesser degree: the visual response was enhanced by MEI = 13±13.5% (mean±s.e.m., P<0.1), and this enhancement was clearly visible in individual experiments (Fig. 3A). As expected, the amplitude of the somatosensory current sink, which preceded the visual response in time, was not affected (MEI = 6.2±8.2%, P>0.9). These results demonstrate a non-linear interaction of visual- and somatosensory-driven responses when the stimuli are presented simultaneously, whereby the somatosensory stimulus enhances the current sink induced by the visual stimulus.


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)

Visual cortex shows less multisensory response.A: The total CSD response to both unimodal stimuli, expressed as averaged rectified CSD (AVREC), confirms the multisensory nature of the investigated parietal region and the near absence of somatosensory-evoked responses in visual cortex. B: CSD responses quantified as the deviation of the measured to the predicted linear multisensory response (SOA = 0 ms, vis&som – (vis+som)). Supra-linear interactions are marked by arrows in the granular (GS) and infra-granular sinks (IS) and also as a late effect in supra-granular layers (LE). Note the absence of multisensory response interactions in visual cortex (right panel, gray arrows mark the same locations as in left panel).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0063631-g003: Visual cortex shows less multisensory response.A: The total CSD response to both unimodal stimuli, expressed as averaged rectified CSD (AVREC), confirms the multisensory nature of the investigated parietal region and the near absence of somatosensory-evoked responses in visual cortex. B: CSD responses quantified as the deviation of the measured to the predicted linear multisensory response (SOA = 0 ms, vis&som – (vis+som)). Supra-linear interactions are marked by arrows in the granular (GS) and infra-granular sinks (IS) and also as a late effect in supra-granular layers (LE). Note the absence of multisensory response interactions in visual cortex (right panel, gray arrows mark the same locations as in left panel).
Mentions: When both stimuli were presented simultaneously (physical stimulus onset asynchrony = 0 ms) the CSD response to the combined stimulus consisted of a leading somatosensory-evoked sink followed by a later visual-evoked sink (Fig. 2A, left), as was expected given the differences in response latencies between the two modalities. Importantly, the somatosensory stimulus (whose activation emerges first) induces a supra-linear enhancement of the amplitude of the visual-evoked current sink; that is, the sink becomes stronger (more negative). This multisensory interaction can be seen in the comparison of the multisensory response and the prediction from the sum of unisensory responses (Fig. 2A, lower panels). The scaled magnitude of this difference is represented by the MEI. The difference between the multisensory response and the unisensory sum was significant across experiments (n = 10, multisensory enhancement index (MEI) = 21.6±4%, mean±s.e.m, Wilcoxon signed rank test: P<0.01, Fig. 2B). A similar effect was seen in the infra-granular sink, albeit to a lesser degree: the visual response was enhanced by MEI = 13±13.5% (mean±s.e.m., P<0.1), and this enhancement was clearly visible in individual experiments (Fig. 3A). As expected, the amplitude of the somatosensory current sink, which preceded the visual response in time, was not affected (MEI = 6.2±8.2%, P>0.9). These results demonstrate a non-linear interaction of visual- and somatosensory-driven responses when the stimuli are presented simultaneously, whereby the somatosensory stimulus enhances the current sink induced by the visual stimulus.

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