Experiments were performed on four European rabbits (Orictolagus cuniculus) and included extracellular recordings of a total of 92 neurons. The first series of experiments recorded the responses of 63 neurons to substitution of visual stimuli presented in pairs (pairs with intensities of 0.28 and 1; 1 and 3; 3 and 6; 6 and 8.5; 8.5 and 14; 14 and 17; and 17 and 20 cd/m2). The same stimulus substitutions were then presented with sound (70 dB, 2000 Hz, 40 msec). Neurons did not respond directly to the sound. Two groups of neurons were found. Responses to “light + sound” complexes (in the interval 40–100 msec from the moment of stimulus substitution) increased by a mean 41% (p < 0.0001) at the lowest stimulus intensities in neurons of group 1 (31%). As light intensity increased, discharges in response to the complex decreased to or even below the level of responses to light. Neurons of group 2 (19%) showed the opposite properties: at low light intensities, responses to complexes were comparable with or even smaller than responses to light, while at high intensities (14–20 cd/m2) responses were significantly different (p < 0.05) from responses to light (by 20–39%). The next series of experiments reconstructed the sensory vector spaces on the basis of the responses to 29 neurons to light stimuli of eight different intensities and “sound + light” complexes. Sound was also found to have a double action on the sensory spaces of complexes. Some neurons showed marked increases in the angular distance between the two lowest-intensity stimuli (0.28 and 1 cd/m2), while others showed an increase in the angular distance for the highest intensities. These changes in the structure of the spaces were consisted with the neuron groups identified in the first two series. Comparison of the dynamics of neuron responses and the amplitudes of evoked potentials in the same stimulation conditions showed that there was significant similarity. Thus, these data lead to the conclusion that modulation of visual cortex neuron activity by sound occurs in a complex, nonlinear manner.
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References
Ch. A. Izmailova, S. A. Isaichev, S. G. Korshunova, and E. N. Sokolov, “Specification of the color and brightness components of visual evoked potentials in humans,” Zh. Vyssh. Nerv. Deyat., 48, No. 5, 777–787 (1998).
V. B. Polyanskii, D. E. Alymkulov, D. V. Evtikhin, et al., “Responses of rabbit visual cortex neurons to changes in the orientation and intensity of visual stimuli,” Zh. Vyssh. Nerv. Deyat., 60, No. 1, 32–43 (2010).
V. B. Polyanskii, D. E. Alymkulov, D. V. Evtikhin, and B. V. Chernyshev, “Sound improves the discrimination of the weakest light intensities in the rabbit visual cortex,” Zh. Vyssh. Nerv. Deyat., 61, No. 5, 595–695 (2011).
V. B. Polyanskii, D. E. Alymkulov, E. N. Sokolov, et al., “Reflection of changes in line orientation and intensity in rabbit visual cortex evoked potentials,” Zh. Vyssh. Nerv. Deyat., 58, No. 6, 688–699 (2008).
V. B. Polyanskii, D. V. Evtikhin, and E. N. Sokolov, “Calculation of color and brightness differences by rabbit visual cortex neurons,” Zh. Vyssh. Nerv. Deyat., 55, No. 1, 60–70 (2005).
V. B. Polyanskii, G. L. Ruderman, E. E. Voronezhskaya, and I. V. Isaev, “Sound-specific neurons in the cat visual cortex,” Zh. Vyssh. Nerv. Deyat., 38, No. 3, 546–549 (1988).
E. N. Sokolov, Perception and Conditioned Reflexes. A New View [in Russian], “Psychology” Educational Methodological Collection, Moscow (2003).
B. L. Allman, L. P. Keniston, and M. A. Meredith, “Subthreshold auditory inputs to extrastriate visual neurons are responsive to parametric changes in stimulus quality: sensory-specific versus non-specific encoding,” Brain Res., 1242, 95–101 (2008).
B. L. Allman, L. P. Keniston, and M. A. Meredith, “Not just for bimodal neurons anymore: the contribution of unimodal neurons to cortical multisensory processing,” Brain Topogr., 21, No. 3–4, 157–167 (2009).
N. Bolognini, I. Senna, A. Maravita, et al., “Auditory enhancement of visual phosphene perception: the effect of temporal and spatial factors and of stimulus intensity,” Neurosci. Lett., 477, No. 3, 109–114 (2010).
E. Budinger, P. Heil, A. Hess, and H. Scheich, “Multisensory processing via early cortical stages: connections of the primary auditory cortical field with other sensory systems,” Neurosci., 143, No. 4, 1065–1083 (2006).
S. Clavagnier, A. Falchier, and H. Kennedy, “Long-distance feedback projections to area V1: implications of multisensory integration, spatial awareness, and visual consciousness,” Cogn. Affect. Behav. Neurosci., 4, No. 2, 117–126 (2004).
D. V. Evtikhin,V. B. Polianskii, D. E. Alymkulov, and E. N. Sokolov, “Coding of luminance and color differences on neurons in the rabbit’s visual system,” Spanish J. Psychol., 11, No. 2, 349–362 (2008).
A. Falchier, S. Clavagnier, P. Barone, and H. Kennedy, “Anatomical evidence of multimodal integration in primate striate cortex,” J. Neurosci., 22, No. 13, 5749–5759 (2002).
R. R. Fay, Hearing in Vertebrates, a Psychophysiological Datebook, Hill-Fay Associates, Winnetka, Illinois (1988), pp. 379–380.
M. C. Fishman and C. R. Michael, “Integration of auditory information in the cat’s visual cortex,” Vision Res., 13, No. 8, 1415–1419 (1973).
J. J. Foxe and C. E. Schroeder, “The case for feedforward multisensory convergence during early cortical processing,” Neuroreport, 16, No. 5, 419–423 (2005).
A. A. Ghazanfar and C. E. Schroeder, “Is neocortex essentially multisensory?” Trends Cogn. Sci., 10, No. 6, 278–285 (2006).
C. Kayser and N. K. Logothetis, “Do early sensory cortices integrate cross-modal information?” Brain Struct. Funct., 212, No. 2, 121–132 (2007).
Q. Liu, J. Qiu, J. Yang, et al., “The effect of visual reliability on auditory-visual integration: an event-related potential study,” Neuroreport, 18, No. 17, 1861–1865 (2007).
T. Lomo and A. Mollica, “Activity of single units in the primary optic cortex in the unanaesthetized rabbit during visual, acoustic, olfactory and painful stimulation,” Arch. Ital. Biol., 100, No. 1, 86–120 (1962).
A. Meienbrock, M. J. Naumer, O. Doehrmann, et al., “Retinotopic effects during spatial audio-visual integration,” Neuropsychologia, 45, No. 3, 531–539 (2007).
F. Morrell, “Specificity of non-visual input to visual cortical neurons,” EEG Clin. Neurophysiol., 31, No. 4, 413–414 (1971).
F. Morrell, “Visual system’s view of acoustic space,” Nature, 238, No. 5358, 44–46 (1972).
K. S. Rockland and H. Ojima, “Multisensory convergence in calcarine visual areas in macaque monkey,” Int. J. Psychophysiol., 50, No. 1–2, 19–26 (2003).
V. Romei, M. M. Murray, L. B. Merabet, and G. Thut, “Occipital transcranial magnetic stimulation has opposing effects on visual and auditory stimulus: implications for multisensory interactions,” J. Neurosci., 27, No. 43, 11465–11472 (2007).
L. Shams,Y. Kamitan, S. Thompson, and S. Shimoto, “Sound alters visual evoked potentials in humans,” Neuroreport, 12, No. 17, 3849–3852 (2001).
D. N. Spinelli, A. Starr, and T. W. Barrett, “Auditory specificity in unit recording from cat’s visual cortex,” Exp. Neurol., 22, No. 1, 75–84 (1968).
B. E. Stein, N. London, L. K. Wilkinson, and D. D. Price, “Enhancement of perceived visual intensity by auditory stimuli: A psychophysical analysis,” J. Cogn. Neurosci., 8, No. 6, 497–506 (1996).
A. M. Wyrwitz, N. Chen, L. Li, et al., “fMRI of visual system activation in conscious rabbit,” Magn. Reson. Med., 44, No. 3, 474–478 (2000).
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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 62, No. 4, pp. 440–452, July–August, 2012.
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Polyanskii, V.B., Alymkulov, D.E., Evtikhin, D.V. et al. Specific Modulation by Sound of Primary Visual Cortex Neuron Responses to Light Stimuli of Different Intensities in Rabbits. Neurosci Behav Physi 43, 1058–1067 (2013). https://doi.org/10.1007/s11055-013-9850-9
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DOI: https://doi.org/10.1007/s11055-013-9850-9