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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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Pharmacological suppression of local activity abolishes non-linear interactions.A: General decrease in average rectified current source density (AVREC) caused by muscimol application (100 ms post-stimulus window, mean of both unisensory stimuli, n = 5, P<0.05, U test). B: Example data showing the bimodal response (vis&som) and the non-linear interaction (vis&som – (vis+som)) for the SOA = 50 ms condition before (upper panel) and after application of muscimol. In the untreated condition, the previously noted pattern of current sinks (left) and sub-linear multisensory interactions are visible (white arrow, right panel). After muscimol application, individual feed-forward current sinks related to visual (arrow V) and somatosensory (arrow S) inputs are apparent, as well as a late additional visual sink (*, bottom left panel). The multisensory interaction is negligible, indicating a linear superposition of responses. Note the different scales in upper and lower panels. C: Peak amplitudes of the visual granular sink during unisensory (vis) and multisensory stimulation (vis (vis&som)) after muscimol treatment do not differ, demonstrating the absence of non-linear interactions. D: Peak amplitudes of the somatosensory granular sink in unisensory (som) and multisensory stimulation (som (vis&som)) after treatment also do not differ, favoring a cortical origin of the observed interactions.
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pone-0063631-g004: Pharmacological suppression of local activity abolishes non-linear interactions.A: General decrease in average rectified current source density (AVREC) caused by muscimol application (100 ms post-stimulus window, mean of both unisensory stimuli, n = 5, P<0.05, U test). B: Example data showing the bimodal response (vis&som) and the non-linear interaction (vis&som – (vis+som)) for the SOA = 50 ms condition before (upper panel) and after application of muscimol. In the untreated condition, the previously noted pattern of current sinks (left) and sub-linear multisensory interactions are visible (white arrow, right panel). After muscimol application, individual feed-forward current sinks related to visual (arrow V) and somatosensory (arrow S) inputs are apparent, as well as a late additional visual sink (*, bottom left panel). The multisensory interaction is negligible, indicating a linear superposition of responses. Note the different scales in upper and lower panels. C: Peak amplitudes of the visual granular sink during unisensory (vis) and multisensory stimulation (vis (vis&som)) after muscimol treatment do not differ, demonstrating the absence of non-linear interactions. D: Peak amplitudes of the somatosensory granular sink in unisensory (som) and multisensory stimulation (som (vis&som)) after treatment also do not differ, favoring a cortical origin of the observed interactions.

Mentions: We applied the GABA-agonist muscimol in combination with the specific GABAB-antagonist SCH50911 to suppress local action potential generation by inducing post-synaptic inhibitory currents (n = 5 experiments). This treatment blocks spiking in all exposed neural elements, except in those originating from outside the treated area. It thereby cancels the contribution of local recurrent connections to the observed CSD patterns. Hence, only afferent synaptic inputs contribute to the CSD. Indeed, the overall CSD response strength as quantified by the AVREC in a 100-ms post-stimulus window (averaged across visual and somatosensory stimuli) was greatly reduced following muscimol application (before treatment: 0.22±0.03 mV/mm2 mean±S.E.; after treatment: 0.0053±0.0012 mV/mm2, U test P<0.01, Fig. 4A). This finding suggests that only 2–3% of the measured activity originates from currents caused by afferent synapses. While this number appears small, one must keep in mind that thalamocortical projections to, for example, the visual cortex account for a similarly small percentage of synapses [84], [85]. Furthermore, the number cortical inter-areal projection synapses is considered to be very small compared to local synapses [86]. Since it is difficult to control the spread of muscimol in the tissue of such a small area, it appears likely that these remaining synapses are mainly thalamocortical and that certainly a number of the intra-cortical connections– if not most – have also been silenced. Nonetheless, this experiment demonstrates that the multisensory effect is not already contained in thalamic input.


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)

Pharmacological suppression of local activity abolishes non-linear interactions.A: General decrease in average rectified current source density (AVREC) caused by muscimol application (100 ms post-stimulus window, mean of both unisensory stimuli, n = 5, P<0.05, U test). B: Example data showing the bimodal response (vis&som) and the non-linear interaction (vis&som – (vis+som)) for the SOA = 50 ms condition before (upper panel) and after application of muscimol. In the untreated condition, the previously noted pattern of current sinks (left) and sub-linear multisensory interactions are visible (white arrow, right panel). After muscimol application, individual feed-forward current sinks related to visual (arrow V) and somatosensory (arrow S) inputs are apparent, as well as a late additional visual sink (*, bottom left panel). The multisensory interaction is negligible, indicating a linear superposition of responses. Note the different scales in upper and lower panels. C: Peak amplitudes of the visual granular sink during unisensory (vis) and multisensory stimulation (vis (vis&som)) after muscimol treatment do not differ, demonstrating the absence of non-linear interactions. D: Peak amplitudes of the somatosensory granular sink in unisensory (som) and multisensory stimulation (som (vis&som)) after treatment also do not differ, favoring a cortical origin of the observed interactions.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3646793&req=5

pone-0063631-g004: Pharmacological suppression of local activity abolishes non-linear interactions.A: General decrease in average rectified current source density (AVREC) caused by muscimol application (100 ms post-stimulus window, mean of both unisensory stimuli, n = 5, P<0.05, U test). B: Example data showing the bimodal response (vis&som) and the non-linear interaction (vis&som – (vis+som)) for the SOA = 50 ms condition before (upper panel) and after application of muscimol. In the untreated condition, the previously noted pattern of current sinks (left) and sub-linear multisensory interactions are visible (white arrow, right panel). After muscimol application, individual feed-forward current sinks related to visual (arrow V) and somatosensory (arrow S) inputs are apparent, as well as a late additional visual sink (*, bottom left panel). The multisensory interaction is negligible, indicating a linear superposition of responses. Note the different scales in upper and lower panels. C: Peak amplitudes of the visual granular sink during unisensory (vis) and multisensory stimulation (vis (vis&som)) after muscimol treatment do not differ, demonstrating the absence of non-linear interactions. D: Peak amplitudes of the somatosensory granular sink in unisensory (som) and multisensory stimulation (som (vis&som)) after treatment also do not differ, favoring a cortical origin of the observed interactions.
Mentions: We applied the GABA-agonist muscimol in combination with the specific GABAB-antagonist SCH50911 to suppress local action potential generation by inducing post-synaptic inhibitory currents (n = 5 experiments). This treatment blocks spiking in all exposed neural elements, except in those originating from outside the treated area. It thereby cancels the contribution of local recurrent connections to the observed CSD patterns. Hence, only afferent synaptic inputs contribute to the CSD. Indeed, the overall CSD response strength as quantified by the AVREC in a 100-ms post-stimulus window (averaged across visual and somatosensory stimuli) was greatly reduced following muscimol application (before treatment: 0.22±0.03 mV/mm2 mean±S.E.; after treatment: 0.0053±0.0012 mV/mm2, U test P<0.01, Fig. 4A). This finding suggests that only 2–3% of the measured activity originates from currents caused by afferent synapses. While this number appears small, one must keep in mind that thalamocortical projections to, for example, the visual cortex account for a similarly small percentage of synapses [84], [85]. Furthermore, the number cortical inter-areal projection synapses is considered to be very small compared to local synapses [86]. Since it is difficult to control the spread of muscimol in the tissue of such a small area, it appears likely that these remaining synapses are mainly thalamocortical and that certainly a number of the intra-cortical connections– if not most – have also been silenced. Nonetheless, this experiment demonstrates that the multisensory effect is not already contained in thalamic input.

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