Sensory inputs from the oral region to the cerebral cortex in behaving rats: an analysis of unit responses in cortical somatosensory and taste areas during ingestive behavior

Abstract

1. The responses of 90 cortical neurons in the somatosensory and gustatory areas were recorded with chronically implanted fine wires in freely moving Wistar rats. The responses were analyzed mainly while the animals were freely licking solutions and eating dry pellets. Cortical neurons were classified into several groups according to their response properties. 2. "Mechanosensitive" neurons (n = 20) showed rhythmic phasic activity in different phases of the licking cycle, depending on the location of their receptive field in the peripheral orofacial region. 3. "Movement-related" neurons (n = 27) changed their activities tonically during licking, chewing, or grooming behavior. The responses were either excitatory or inhibitory. Receptive fields and adequate stimuli could not be identified. These neurons might receive somatosensory (except light tactile) inputs from wide or deep areas of intra- or perioral regions, or might be related to orofacial active movement. 4. "Taste" neurons (n = 35) increased or decreased their discharge rates during licking of particular taste solutions. Some taste neurons received convergence from somatosensory inputs. 5. "Temperature" neurons (n = 2) responded exclusively to water of temperatures lower or higher than room temperature. The responses were opposite in direction between cold and warm stimuli. 6. "Anticipation" neurons (n = 4) increased their impulse discharges before the start of licking in the situation in which the animal expected access to the drinking tube. 7. "Attention" neurons (n = 2) responded to arousal stimulation such as sound, a flash of light, and body touch. These neurons showed only a slightly increasing response during ingestive behavior. 8. The locations of 56 of 90 units were histologically identified. Mechanosensitive neurons were located in the appropriate parts of the somatotopic pattern within the primary somatic sensory area in the granular cortex. Taste neurons were found evenly in the dysgranular cortex and the agranular insular cortex. Other types of neurons were located mainly in the dysgranular cortex between the granular cortex and agranular insular cortex, and some were intermingled with taste neurons in the agranular insular cortex. 9. The present study has shown that cortical neurons in the orolingual somatosensory and taste areas have different response characteristics related to each aspect of ingestive behavior.(ABSTRACT TRUNCATED AT 400 WORDS)

Neural mechanisms of nociception during orthodontic treatment

“…Yamamoto et al (47) reported that in the rat a subset of neurons in the insular cortex (IC) responds to mechanical stimulation of oral structures. In agreement with this study, a functional magnetic resonance imaging (fMRI) study of humans reported activation of the IC and supplementary motor cortex during vibratory stimulation of teeth (48).…”

Learning-Related Plasticity of Temporal Coding in Simultaneously Recorded Amygdala–Cortical Ensembles

“…Some neurons in GC respond to somatosensory stimulation of the tongue and oral cavity (Yamamoto et al, 1988). These neurons fire action potentials synchronized to the rhythmic (6 -9 Hz) licking behavior produced by the rat during taste sampling (Katz et al, 2001a).…”

Differential Columnar Processing in Local Circuits of Barrel and Insular Cortices

“…In the insular cortex, a variety of neurons that respond to taste, tactile, thermal, or nociceptive stimulation (Cechetto and Saper, 1987;Yamamoto et al, 1988;Allen et al, 1991;Hanamori et al, 1998) were layer-specifically distributed. Tasteresponsive neurons together with low-threshold mechanoreceptive and wide-dynamic range neurons were mainly identified in layer V, whereas nociceptive-specific neurons were in layer II/III (Wang and Ogawa, 2002).…”

“…Indeed, there were considerable overlaps among the representation areas of the four basic tastes in rats (Accolla et al, 2007). The taste neurons are intermingled with sensory neurons for various other modalities such as tactile, thermal, and nociceptive sensations (Cechetto and Saper, 1987;Yamamoto et al, 1988;Allen et al, 1991;Hanamori et al, 1998). Furthermore, the gustatory insular cortex is mainly composed of dysgranular and agranular cortices, thereby displaying either a thin layer IV or no layer IV (Yamamoto et al, 1984).…”