Physiological and Anatomical Organization of Multiwhisker Response Interactions in the Barrel Cortex of Rats

Shimegi, Satoshi; Akasaki, Takafumi; Ichikawa, Takehiko; Sato, Hiromichi

doi:10.1523/jneurosci.20-16-06241.2000

Cited by 59 publications

(102 citation statements)

References 39 publications

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“…Despite the predominance of suppressive interactions that we have observed, previous studies on the spatiotemporal sensory integration performed by barrel cortex neurons have reported the presence of facilitatory interactions between the responses for different whiskers (Ghazanfar and Nicolelis 1997;Ghazanfar et al 2000;Shimegi et al 1999Shimegi et al , 2000. Notably, the work by Shimegi and colleagues, using very similar procedures to those applied here (anesthesia, unit recording, frequency of stimulation, choice of ISIs), has described a much higher incidence of supralinear summation for 0.5-Hz stimulation than what we have observed.…”

Section: Incidence Of Supralinear Interactions For Stimulation At a Lcontrasting

confidence: 60%

“…Additionally, unit recording (ArmstrongJames and Fox 1987;Simons 1978) and optical imaging (Kleinfeld and Delaney 1996) studies have reported activity patterns in the barrel cortex following single-whisker deflections elongated along rows. In line with those results, electrophysiological investigations have mainly tested multi-whisker integration along rows (Carvell and Simons 1988;Shimegi et al 1999Shimegi et al , 2000Simons 1985;Simons and Carvell 1989; but see also Mirabella et al 2001). However, a supralinear interaction most prominent for whiskers located in the same arc was recently described (Ghazanfar and Nicolelis 1997), suggesting that modulatory influences could exist both in the rostrocaudal and dorsoventral directions.…”

Section: Introductionmentioning

confidence: 70%

“…First, we calculated the facilitation index (FI) proposed by Shimegi et al (1999Shimegi et al ( , 2000. The FI is the ratio between the observed response to the combined deflection of whiskers and the sum of responses to individual deflections calculated on the same time window.…”

Section: Discussionmentioning

confidence: 99%

“…These investigations have mostly reported a suppressive effect of the stimulation of one whisker on the response to stimulation of another whisker, using both electrophysiological recordings (Brumberg et al 1996;Carvell and Simons 1988;Mirabella et al 2001;Simons 1985;Simons and Carvell 1989) and optical imaging techniques (Goldreich et al 1998;Kleinfeld and Delaney 1996). However, a facilitatory interaction has also been described by several laboratories (Erchova et al 2003;Ghazanfar and Nicolelis 1997;Ghazanfar et al 2000;Shimegi et al 1999Shimegi et al , 2000. These apparently conflicting results could arise from several differences in the experimental protocols used, namely the range of interstimulus intervals (ISIs), the laminar location of the recordings, and the type of recorded neurons.…”

Section: Introductionmentioning

confidence: 99%

“…However, a supralinear interaction most prominent for whiskers located in the same arc was recently described (Ghazanfar and Nicolelis 1997), suggesting that modulatory influences could exist both in the rostrocaudal and dorsoventral directions. Because the effect of the deflection of one whisker on the response to the deflection of another whisker depends on the precise ISI (Shimegi et al 1999(Shimegi et al , 2000, it becomes critical to test multi-whisker integration both along rows and arcs with a range of ISIs.…”

Section: Introductionmentioning

confidence: 99%

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Spatiotemporal Characteristics of Neuronal Sensory Integration in the Barrel Cortex of the Rat

Ego-Stengel¹,

Souza²,

Jacob³

et al. 2005

Journal of Neurophysiology

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. Spatiotemporal characteristics of neuronal sensory integration in the barrel cortex of the rat. J Neurophysiol 93: 1450 -1467, 2005. First published October 20, 2004 doi:10.1152/ jn.00912.2004. In primary sensory cortices, neuronal responses to a stimulus presented as part of a rapid sequence often differ from responses to an isolated stimulus. It has been reported that sequential stimulation of two whiskers produces facilitatory modulations of barrel cortex neuronal responses. These results are at odds with the well-known suppressive interaction that has been usually described. Herein, we have examined the dependency of response modulation on the spatiotemporal pattern of stimulation by varying the spatial arrangement of the deflected vibrissae, the temporal frequency of stimulation, and the time interval between whisker deflections. Extracellular recordings were made from primary somatosensory cortex of anesthetized rats. Two contralateral whiskers were stimulated at 0.5 and 8 Hz at intervals ranging from 0 to Ϯ30 ms. Response interactions were assessed during stimulation of the principal and adjacent whiskers, first from the same row and second from the same arc. When tested at 0.5 Hz, 59% of single units showed a statistically significant suppressive interaction, whereas response facilitation was found in only 6% of cells. In contrast, at 8 Hz, a significant supralinear summation was observed in 19% of the cells, particularly for stimulations along an arc rather than along a row. Multi-unit recordings showed similar results. These observations indicate that most of the interactions in the barrel cortex during two-whisker stimulation are suppressive. However, facilitation can be revealed when stimuli are applied at a physiological frequency and could be the basis for internal representations of the spatiotemporal pattern of the stimulus.

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Section: Incidence Of Supralinear Interactions For Stimulation At a Lcontrasting

confidence: 60%

Section: Introductionmentioning

confidence: 70%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Spatiotemporal Characteristics of Neuronal Sensory Integration in the Barrel Cortex of the Rat

Ego-Stengel¹,

Souza²,

Jacob³

et al. 2005

Journal of Neurophysiology

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Similarities and differences in the innervation of mystacial vibrissal follicle–sinus complexes in the rat and cat: A confocal microscopic study

Ebara

Kumamoto

Matsuura

et al. 2002

J of Comparative Neurology

276

254

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Our confocal three-dimensional analyses revealed substantial differences in the innervation to vibrissal follicle-sinus complexes (FSCs) in the rat and cat. This is the first study using anti-protein gene product 9.5 (PGP9.5) immunolabeling and confocal microscopy on thick sections to examine systematically the terminal arborizations of the various FSC endings and to compare them between two species, the rat and the cat, that have similar-appearing FSCs but different exploratory behaviors, such as existence or absence of whisking. At least eight distinct endings were clearly discriminated three dimensionally in this study: 1) Merkel endings at the rete ridge collar, 2) circumferentially oriented lanceolate endings, 3) Merkel endings at the level of the ring sinus, 4) longitudinally oriented lanceolate endings, 5) club-like ringwulst endings, 6) reticular endings, 7) spiny endings, and 8) encapsulated endings. Of particular contrast, each nerve fiber that innervates Merkel cells at the level of the ring sinus in the rat usually terminates as a single, relatively small cluster of endings, whereas in the cat they terminate en passant as several large clusters of endings. Also, individual arbors of reticular endings in the rat ramify parallel to the vibrissae and distribute over wide, overlapping territories, whereas those in the cat ramify perpendicular and terminate in tightly circumscribed territories. Otherwise, the inner conical body of rat FSCs contains en passant, circumferentially oriented lanceolate endings that are lacking in the cat, whereas the cavernous sinus of the cat has en passant corpuscular endings that are lacking in the rat. Surprisingly, the one type of innervation that is the most similar in both species is a major set of simple, club-like endings, located at the attachment of the ringwulst, that had not previously been recognized as a morphologically unique type of innervation. Although the basic structure of the FSCs is similar in the rat and cat, the numerous differences in innervation suggest that these species would have different tactile capabilities and perceptions possibly related to their different vibrissa-related exploratory behaviors.

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Postnatal growth of intrinsic connections in mouse barrel cortex

Miller

Blake

Erinjeri

et al. 2001

J of Comparative Neurology

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Surprisingly little is known about the development of connections within a functional area of the cerebral cortex. We examined the postnatal growth of connections in mouse barrel cortex during the second and third weeks after birth, coinciding with the period of rapid synaptogenesis that occurs just after the barrels first form. A barrel is a group of neurons in layer 4 of somatosensory cortex that is part of a cortical column. Each whisker/barrel column is linked anatomically and functionally to a homotopic whisker on the contralateral face. Radial groups of cortical neurons were labeled with the neuronal tracer biotinylated dextran amine in mice ranging in age from postnatal day 8 (P8; P0 is the date of birth) to adulthood. The spatial distributions of retrogradely labeled neurons in different laminae were analyzed. The barrel map in layer 4 was used as a template to compare quantitative data from different animals and to account for substantial changes in barrel and barrel field size during development. Intrinsic projections 1) innervate increasingly more distant targets within barrel cortex up to 3 weeks of age; 2) continue to form in targets after 3 weeks, effectively strengthening existing connections; 3) follow a timetable for growth that is layer-specific; 4) link more distant barrel columns in layer 4 from neurons that are found preferentially in the barrel side and the septa between barrels; and 5) form over the shortest distances between the barrel columns. These data indicate that intrinsic connections in mouse barrel cortex develop by the progressive addition of neuronal connections rather than by sculpting preliminary connections. We describe statistically significant changes in connectivity during development that may be applied to model and assess the development of connections after a variety of experimental perturbations, such as to the environment and/or the genome.

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Physiological and Anatomical Organization of Multiwhisker Response Interactions in the Barrel Cortex of Rats

Cited by 59 publications

References 39 publications

Spatiotemporal Characteristics of Neuronal Sensory Integration in the Barrel Cortex of the Rat

Spatiotemporal Characteristics of Neuronal Sensory Integration in the Barrel Cortex of the Rat

Similarities and differences in the innervation of mystacial vibrissal follicle–sinus complexes in the rat and cat: A confocal microscopic study

Postnatal growth of intrinsic connections in mouse barrel cortex

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