Kayoko Hasegawa

Taste area in granular and dysgranular insular cortices in the rat identified by stimulation of the entire oral cavity

While applying natural stimulation to the entire oral cavity, we recorded responses from 489 neurons (400 mechanoreceptive, 84 taste and 5 cold neurons) in the insular cortex of urethane-anesthetized rats. Intermingled with the mechanoreceptive neurons was a major group of taste neurons located in the granular or dysgranular insular area at levels of 2.55-1.20 mm anterior to the bed nucleus of the anterior commissure as stereotaxically located. Most of the taste neurons were also sensitive to mechanical stimulation of the oral and/or perioral tissue.

Difference in taste quality coding between two cortical taste areas, granular and dysgranular insular areas, in rats

SummaryThe responses of 84 taste neurons to stimulation of the oral cavity in rats were examined; most taste neurons were found in either a granular insular area (area GI; n = 55) or dysgranular insular area (DI; n = 25), and the others (n = 4) were in an agranular insular area (area AI). The fraction of neurons responding to only one of the four basic stimuli was significantly larger in area GI than in area DI. When neurons were classified by the stimulus which most excited the neuron among the four basic stimuli, every “best-stimulus category” of neurons was found in both GI and DI areas. Quinine-best and “multistimulus-type” neurons, whose responses to some non-best stimulus exceeded 90% of the maximum, were more numerous in the cortex than in the thalamocortical relay neurons. When responses were plotted against taste stimuli arranged in the order of sucrose, NaCl, HCl, and quinine along the abscissa (taste coordinate), response profiles of taste neurons often showed two peaks. The double-peaked type of response profiles were found in every best-stimulus category of neurons in both areas; though, a significantly large fraction of quinine-best neurons in area GI were of the double-peaked type. Some taste neurons in area GI (n = 21) and in area DI (n = 7) were inhibited by one to two taste stimuli, particularly by the stimuli present next to the best one along the taste coordinate. In correlation profiles — correlation coefficients between sucrose and NaCl and between HCl and quinine — pairs of stimuli which were located next to each other on the taste coordinate were significantly smaller in area GI than in area DI. It is thus highly probable that area GI plays an important role in fine taste discrimination and area DI in integration of taste information.

GABAergic inhibition and modifications of taste responses in the cortical taste area in rats

Using multibarrel electrodes, recordings were made in the cortical taste area (CTA), specifically in the granular and dysgranular parts of the insular cortex (areas GI and DI), of urethane-anesthetized rats. The effects of an iontophoretic application of gamma-aminobutylic acid (GABA) and bicuculline methiodide (BMI), a specific antagonist to the GABA(A) receptor, were tested. GABA decreased background discharges in ca. 69% of 509 neurons in both areas, and in ca. 58% of 64 taste neurons. BMI antagonized the inhibitory action of GABA in CTA neurons and facilitated background discharges in ca. 51% of the 390 neurons tested, including ca. 69% of the 52 taste neurons, which indicates that CTA neurons have GABA(A) receptors to receive inhibitory inputs from interneurons. In both areas, the effects of BMI (6-20 nA) on taste responses of the 85 CTA neurons (49 and 36 in areas GI and DI, respectively) to the four basic taste stimuli were examined: 65 neurons were recognized in the absence of BMI, whereas 20 only in the presence of the drug. BMI increased taste responses in 25 of the former group and changed the type of their response profiles in 25 including 12 neurons whose responses were increased. It also changed the best stimulus in 34 neurons. The drug affected the receptive fields in almost all cases examined (n = 23) and increased the size in 78.2% when the value for all four basic taste stimuli were totaled. New receptive fields were uncovered by BMI in varying regions of the oral cavity depending on the taste stimulus. But the drug decreased taste responses in several neurons (n = 8). These findings indicate that the GABAergic inhibitory system apparently contributes to modifying or selecting taste information in both areas of the CTA.

Difference in receptive field features of taste neurons in rat granular and dysgranular insular cortices

SummaryReceptive fields (RFs) of 59 cortical taste neurons (35 in the granular insular area, area GI, 21 in the dysgranular insular area, area DI, and 3 in the agranular insular area, area AI) were identified in the oral cavity of the rat. The fraction of the neurons with RFs in the anterior oral cavity only was significantly larger in area GI (74.3%) than in area DI (42.9%). On the other hand, the fraction of neurons with RFs in both the anterior and posterior oral cavity was larger in area DI (42.9%) than in area GI (11.4%). On the whole, it is suggested that area GI is involved in discrimination of several taste stimuli in the oral cavity, whereas in area DI taste information originating from various regions of the oral cavity is integrated. When neurons were classified according to the best stimulus which most excited the neuron among the four basic tastes, different categories of taste neurons had RFs in different parts of the oral cavity. It is suggested that, in either taste area, different categories of taste neurons are involved in different sorts of taste coding. The majority of neurons in both areas had bilateral RFs. In area GI, neurons with RFs on single subpopulations of taste buds were significantly more numerous at the rostral region of the cortex than at the caudal region. There was no such relation between RF types and cortical localization in area DI. Otherwise, topographic representation of the oral cavity by taste neurons on the cortical surface was not obvious. RF features of taste neurons did not differ across layers in either cortical area.

Identification and characterization of an insular auditory field in mice

We used voltage‐sensitive‐dye‐based imaging techniques to identify and characterize the insular auditory field (IAF) in mice. Previous research has identified five auditory fields in the mouse auditory cortex, including the primary field and the anterior auditory field. This study confirmed the existence of the primary field and anterior auditory field by examining the tonotopy in each field. Further, we identified a previously unreported IAF located rostral to known auditory fields. Pure tone evoked responses in the IAF exhibited the shortest latency among all auditory fields at lower frequencies. A rostroventral to dorsocaudal frequency gradient was consistently observed in the IAF in all animals examined. Neither the response amplitude nor the response duration changed with frequency in the IAF, but the area of activation exhibited a significant increase with decreasing tone frequency. Taken together, the current results indicate the existence of an IAF in mice, with characteristics suggesting a role in the rapid detection of lower frequency components of incoming sound.

The insular auditory field receives input from the lemniscal subdivision of the auditory thalamus in mice.

The insular cortex plays important roles in vocal communication, but the origin of auditory input to the insular cortex has not been fully clarified. Here we studied the auditory thalamic input to the insular cortex using mice as a model system. An insular auditory field (IAF) has recently been identified in mice. By using retrograde neuronal tracing, we identified auditory thalamic neurons projecting to the IAF, primary auditory cortex (AI), and anterior auditory field (AAF). After mapping the IAF, AAF, and AI by using optical imaging, we injected a distinct fluorescent tracer into each of the three fields at frequency‐matched locations. Tracer injection into the IAF resulted in retrogradely labeled cells localized ventromedially in the lemniscal division, i.e., the ventral subdivision of the medial geniculate body (MGv). Cells retrogradely labeled by injections into the AAF were primarily found in the medial half of the MGv, whereas those from AI injections were located in the lateral half, although some of these two subsets were intermingled within the MGv. Interestingly, retrogradely labeled cells projecting to the IAF showed virtually no overlap with those projecting to the AAF or the AI. Dual tracer injections into two sites responding to low‐ and high‐frequency tones within each of the three auditory fields demonstrated topographic organizations in all three thalamocortical projections. These results indicate that the IAF receives thalamic input from the MGv in a topographic manner, and that the MGv–IAF projection is parallel to the MGv–AAF and MGv–AI projections. J. Comp. Neurol. 522:1373–1389, 2014.

Differential development of cortical taste areas in granular and dysgranular insular cortices in rats.

Recordings were made from taste neurons in granular and dysgranular areas of the insular cortex of anesthetized SD-rats from the age of 4 days to over 90 days (adults). Almost all of the taste neurons were detected in the dysgranular area prior to weaning, but the number in the granular area increased with age and exceeded the number in the dysgranular area after the age of 50 days. In the dysgranular area, most taste neurons, irrespective of the postnatal age, were located at layer 5. However, in the granular area they were found at a deeper layer, with the advance in age; e.g. layer 2-3 at 14-20 days to layer 5 in adults. Thus, taste afferents in granular and dysgranular areas of the insular cortex differ with advance in age.

Effects of acetylcholine on coding of taste information in the primary gustatory cortex in rats

Acetylcholine (ACh) receptors are widely distributed throughout the cerebral cortex in rats. Recently, cholinergic innervation of the gustatory cortex (GC) was reported to be involved in certain taste learning in rats. Here, the effects of iontophoretic application of ACh on the response properties of GC neurons were studied in urethane-anesthetized rats. ACh affected spontaneous discharges in a small fraction of taste neurons (11 of 86 neurons tested), but influenced taste responses in 27 of 43 neurons tested. No correlations with ACh susceptibility were noted for spontaneous discharges and taste responses. Among the 27 neurons, ACh facilitated taste responses in 13, inhibited taste responses in 13 and either facilitated or inhibited taste responses depending on the stimuli in 1. Furthermore, ACh affected the responses to best stimuli that produced the largest responses among four basic tastants (best responses) in 7 of 27 taste neurons, to non-best responses in 9, and to both best and non-best responses in 11. ACh mostly inhibited the best responses (13 of 18 neurons). Thus, ACh often decreased the response selectivity to the four basic tastants and changed the response profile. Atropine, a general antagonist of muscarinic receptors, antagonized ACh actions on taste responses or displayed the opposite effects on taste responses to ACh actions in two-thirds of the neurons tested. These findings indicate that ACh mostly modulates taste responses through muscarinic receptors, and suggest that ACh shifts the state of the neuron network in the GC, in terms of the response selectivities and response profiles.

Handedness: dependent asymmetrical location of the human primary gustatory area, area G.

In magnetoencephalogram studies, the primary gustatory area, area G, is not always seen in the same coronal plane in both hemispheres. We investigated possible asymmetry in right-handed and left-handed individuals by functional MRI. Group analyses revealed a significant difference in the antero-posterior coordinates of the area G between the right and left hemispheres in the right-handed group, but not in the left-handed group, indicating significant morphometric asymmetry in the former group and ambiguous morphometric asymmetry in the latter. However, in left-handed individuals with motor speech areas detected in the right hemisphere, area G was more posteriorly located in the right than in the left hemisphere. These findings suggest that the motor speech area contributes to the asymmetric location of area G.

Comparison of the Upper Marginal Neurons of Cortical Layer 2 with Layer 2/3 Pyramidal Neurons in Mouse Temporal Cortex

Layer 2/3 (L2/3) excitatory neurons in the neocortex make major contributions to corticocortical connections and therefore function to integrate information across cortical areas and hemispheres. Recent evidence suggests that excitatory neurons in L2/3 can have different properties. Sparse evidence from previous studies suggests that L2 neurons located at the border between L1 and L2 (referred to as L2 marginal neurons, L2MNs), have a morphology distinct from a typical pyramidal neuron. However, whether the membrane properties and input/output properties of L2MNs are different from those of typical pyramidal neurons in L2/3 is unknown. Here we addressed these questions in a slice preparation of mouse temporal cortex. We found that L2MNs were homogeneous in intrinsic membrane properties but appeared diverse in morphology. In agreement with previous studies, L2MNs either had oblique apical dendrites or had no obvious apical dendrites. The tufts of both apical and basal dendrites of these neurons invaded L1 extensively. All L2MNs showed a regular firing pattern with moderate adaptation. Compared with typical L2/3 pyramidal neurons that showed regular spiking (RS) activity (neurons), L2MNs showed a higher firing rate, larger sag ratio, and higher input resistance. No difference in the amplitude of excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs, respectively), evoked by stimulation of L1, was found between the two types of neurons, but the IPSPs in L2MNs had a slower time course than those in L2/3 RS cells. In paired recordings, unitary EPSPs showed no significant differences between synapses formed by L2MNs and those formed by L2/3 RS neurons. However, short-term synaptic depression (STSD) examined with a L2MN as the presynaptic neuron was greater when another L2MN was the postsynaptic neuron than when a L2/3 RS neuron was the postsynaptic neuron. The distinct morphological features of L2MNs found here have developmental implications, and the differences in electrophysiological properties between L2MNs and other L2/3 pyramidal neurons suggest that they play different functional roles in cortical networks.