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The insula: anatomic study and MR imaging display at 1.5 T.

BACKGROUND AND PURPOSE: The insula is important for gustatory sensation, motor speech control, vestibular function, and sympathetic control of cardiovascular tone. The purpose of this study was to test two hypotheses: 1) gross anatomic study of the insula will disclose reproducible patterns of insular structure, and 2) analysis of MR appearance will enable physicians to recognize these patterns on imaging studies. METHODS: Gross insular anatomy was determined in 16 normal human cadaveric hemispheres. The 1.5-T MR images of 300 insulae were analyzed to determine the gyral and sulcal patterns displayed; their relationship to the Heschl gyrus, to the overlying opercula, and to the vertical planes perpendicular to the Talairach-Tournoux baseline at the anterior commissure (VAC) and posterior commissure (VPC); their continuity into the orbitofrontal cortex; and appropriate landmarks for the anterior border, apex, and posterior border of the insula. RESULTS: MR images displayed the central sulcus of the insula (97%); the anterior (99%), middle (78%), and posterior (98%) short insular gyri that converge to the apex (100%) anteriorly; and the anterior (99%) and posterior (58%) long insular gyri posteriorly. The middle short gyrus was often hypoplastic (33%). The anterior intersections of the internal and external capsules typically delimit the anterior insular border (87%). VAC intersects the anterior insula (99%), usually at the precentral sulcus. The Heschl gyrus circumscribes the posteroinferior insula (100%). VPC demarcates the posterior insular border (94%). CONCLUSION: The two hypotheses were proved correct. The insula shows reproducible patterns of gross anatomy that are demonstrable on routine clinical MR images obtained at 1.5 T.

Adolescent↗

Taste pathways that mediate accumbens dopamine release by sapid sucrose.

Although it has been associated with the release of dopamine in the forebrain, reward remains a conundrum in neuroscience. Sucrose is inherently rewarding and its sensory message reaches the brain via the gustatory system. In rodents, the central gustatory system bifurcates in the pontine parabrachial nuclei, one arm forming a standard thalamocortical axis, the other distributing widely in the limbic forebrain. We report here that lesions of the gustatory thalamus fail to affect dopamine overflow during sucrose licking (149+/-5% vs. 149+/-4% for controls). Similar damage to the parabrachial nuclei, which severs the limbic taste projection, substantially reduces dopamine release from the nucleus accumbens (121+/-4% vs. 168+/-9% for sham operated controls; p<0.02). This represents the first demonstration that the affective character of a sensory stimulus might separate from the thalamocortical system as early as the second central synapse.

Animals↗

Conditioned taste aversion elicited by intracerebral administration of drugs.

Conditioned taste aversion (CTA) is a vital adaptive reaction governed by highly reliable but poorly understood central mechanisms. In an attempt to elucidate the site of action of various CTA eliciting drugs, equipotent dosages were applied by the systemic (i.p.) and intracerebral (i.c.) route. Rats were offered water on days 1 and 2. On day 3 they received 0.1% sodium saccharin (CS) followed by pentobarbital anaesthesia and i.p. or i.c. injection of the drug (US). After water on day 4, the rats were allowed to choose between water and saccharin on day 5. The putative central action of amphetamine was not confirmed by this experimental arrangement, since CTA was evoked by only moderately (about 10 times) lower i.c. than i.p. dosages. Similar ratio of the i.c. to i.p. effective dosages was obtained with carbachol. On the other hand, CTA of clearly central origin was caused by harmaline and by other monoamine oxidase inhibitors, pargyline and clorgyline, which elicited comparable aversion using 500, 400 and 250 times lower i.c. than i.p. dosages, respectively. The intracerebral gradient of the effect pointed to the lower medulla (inferior olive, raphe nuclei) as the critical brain region and to serotonin as the transmitter participating in the aversive labeling of the gustatory stimulus. The CTA-forming mechanism can also be studied by analysing the action of drugs, e.g. convulsants, which do not produce CTA even when applied at highly toxic dosages (LD 50) eliciting long lasting convulsions (picrotoxin, 5 mg/kg; bicuculline, 5 mg/kg). It is concluded that comparison of brain events elicited by drugs which can or cannot serve as unconditioned stimuli in the CTA paradigm may substantially contribute to the exploration of the underlying neural mechanisms.

Animals↗

Differential effects of glucocorticoids on human auditory perception.

It is assumed that glucocorticoids and mineralocorticoids, the hormones produced by the adrenal cortex, act as modulators of central nervous functions in addition to their well-known role in endocrine stress responses. More specifically, it has been suggested that adrenal corticoids cause changes in sensory thresholds. In two double-blind crossover studies we evaluated auditory perception in healthy volunteers after treatment with hydrocortisone, dexamethasone, and the respective placebos. Stapedial reflexes, pure tone and speech audiograms, and brainstem electric response audiometry served as the dependent variables. As circadian changes in the density and occupancy of the brain corticosteroid receptors have been postulated, we performed Study I in the morning and Study II in the evening. Treatment effects clearly varied with time of day. A differential effect of the two corticoids occurred on contralateral stapedial reflexes. These results parallel results obtained with gustatory stimuli, and suggest that glucocorticoids modulate sensory perception across modalities.

Adult↗

On-line psychophysical data acquisition and event-related fMRI protocol optimized for the investigation of brain activation in response to gustatory stimuli.

An experimental method for event-related functional magnetic resonance imaging that allows for the presentation of several chemosensory stimuli in the oral cavity during the same run, the collection of psychophysical measures (intensity or pleasantness) during the presentation of the stimuli, and the analysis of the data in an event-related fashion are described. The automatic pumps used to present taste stimuli allowed for multiple tastes to be delivered in small amounts under computer control. Psychophysical ratings of pleasantness or intensity were collected after each presentation of a taste stimulus and water, with the general labeled magnitude scale, using a joystick that controlled the movement of an arrow on the visual display. Performing these cognitive tasks required that the participant remained focused, and aided in the interpretation of the data collected. The perceived pleasantness differed across stimuli for all conditions; however, pleasantness ratings for the same stimulus displayed consistency, over the duration of the run and before each scan on separate days. Activation in response to sucrose and caffeine while the participant rated pleasantness was found in the insula, frontal operculum, rolandic operculum and orbitofrontal cortex which is consistent with previous taste fMRI studies.

Adult↗

[The neural bases of taste aversion learning: the formation of acquired hedonic taste representations].

INTRODUCTION: Taste aversion conditioning is a form of associative learning in which certain qualities of a food (mainly its taste) are associated to specific negative visceral consequences that derive from eating it. Establishing this learning depends on gustatory-visceral integration processes carried out in the central nervous system. DEVELOPMENT: In this manuscript our aim is to offer a global view of the centres and connections that play the most significant roles in the formation of taste aversion learning (TAL). CONCLUSIONS: Many researchers consider that the initial level of integration is situated within the parabrachial nuclei. A priori and given the basic vital nature of TAL, its formation and completion could be thought to take place at this brain stem level, without requiring the intervention of the higher processing structures. Nevertheless, in the literature on TAL there is a large body of both neuroanatomical and neurobehavioural evidence that seems to indicate that the formation of TAL requires complex interactions between the parabrachial nuclei and certain prosencephalic structures, such as the insular cortex or the amygdala, among others.

Amygdala↗

Gastrointestinal reactivity in rats lacking anterior insular neocortex.

Behavioral and physiological studies have shown that the insular neocortex participates in a wide variety of special visceral processes, in particular, the higher-order integration of taste stimuli and the regulation of autonomic activity. The present experiment examined the involvement of the anterior insular (gustatory) neocortex (AIGN) in gastrointestinal reactivity and taste learning in rats by the use of a modified taste aversion training procedure. Normal rats and rats lacking AIGN demonstrated similar "illness thresholds" to the early onset symptoms of ingested LiCl. Conversely, animals lacking AIGN showed significant impairments in taste aversion learning ability. From a consideration of several research findings it is concluded that animals lacking AIGN can normally perceive tastes and illness, but these animals experience reliable impairments in taste aversion learning ability.

Animals↗

Seizures produced by pilocarpine in mice: a behavioral, electroencephalographic and morphological analysis.

Increasing doses of pilocarpine, 100-400 mg/kg, were given intraperitoneally to mice and the resulting behavioral, electroencephalographic and neuropathological alterations were studied. No behavioral phenomena were observed in mice treated with the lowest dose of pilocarpine. Occasional tremor and myoclonus of hindlimbs were found in animals which received pilocarpine in a dose of 200 mg/kg. At doses of 300, 325 and 350 mg/kg, pilocarpine produced a sequence of behavioral alterations including staring spells, limbic gustatory automatisms and motor limbic seizures that developed over 15-30 min and built up progressively into a limbic status epilepticus lasting for several hours. The highest dose of pilocarpine, 400 mg/kg, was generally lethal to mice. Pilocarpine produced both interictal and ictal epileptiform activity in the electroencephalogram (EEG). The earliest EEG alterations appeared in the hippocampus and then spread to cortical areas. EEG seizures started 10-15 min after injection of large doses of pilocarpine, 300-350 mg/kg. Ictal periods lasted for 1-2 min, recurred every 5-10 min and were followed by periods of depression of the EEG activity. By 30-45 min paroxysmal activity resulted in a status epilepticus. Examination of frontal forebrain sections with light microscopy revealed a widespread damage to several brain regions including the hippocampus, amygdala, thalamus, olfactory cortex, neocortex and substantia nigra. Scopolamine, 10 mg/kg, and diazepam, 10 mg/kg, prevented the development of convulsive activity and brain damage produced by pilocarpine. The results emphasize that excessive and sustained stimulation of cholinergic receptors can lead to seizures and seizure-related brain damage in mice. It is proposed that systemic pilocarpine in mice provides a useful animal model for studying mechanisms of and therapeutic approaches to temporal lobe epilepsy.

Animals↗

Two distinct projection areas from tongue nerves in the frontal operculum of macaque monkeys as revealed with evoked potential mapping.

Projection areas in the cerebral cortex from tongue nerves were investigated in anesthetized macaque monkeys (Macaca fuscata). Three tongue nerves (lingual nerve, chorda tympani, and a lingual branch of the glossopharyngeal nerve) were electrically stimulated and thereby evoked mass field potentials were recorded with microelectrodes roving through the exposed and buried frontal operculum. Two distinct tongue nerve projection areas were thus located; one in the lower part of the precentral gyrus ventral to the inferior precentral sulcus, and the other in the medial part of the buried frontal operculum. The former corresponds to the "cortical masticatory area", previously defined in macaque monkeys as involved in somatic sensation as well as mastication. However, the prominent projection from the chorda tympani and glossopharyngeal nerve branch, containing taste fibers, to this area suggests its involvement in taste sensation. The latter corresponds to the "pure gustatory area" defined in squirrel monkeys in both location and cytoarchitecture. However, projection to this area from the lingual nerve, which contains only somatic nerve fibers, suggests its involvement in somatic sensation, as well.

Animals↗

[The nucleus tractus solitarius: neuroanatomic, neurochemical and functional aspects].

The nucleus tractus solitarii (NTS) has long been considered as the first central relay for gustatory and visceral afferent informations only. However, data obtained during the past ten years, with neuroanatomical, biochemical and electrophysiological techniques, clearly demonstrate that the NTS is a structure with a high degree of complexity, which plays, at the medullary level, a key role in several integrative processes. The NTS, located in the dorsomedial medulla, is a structure of small size containing a limited number of neurons scattered in a more or less dense fibrillar plexus. The distribution and the organization of both the cells and the fibrillar network are not homogeneous within the nucleus and the NTS has been divided cytoarchitectonically into various subnuclei, which are partly correlated with the areas of projection of peripheral afferent endings. At the ultrastructural level, the NTS shows several complex synaptic arrangements in form of glomeruli. These arrangements provide morphological substrates for complex mechanisms of intercellular communication within the NTS. The NTS is not only the site of vagal and glossopharyngeal afferent projections, it receives also endings from facial and trigeminal nerves as well as from some renal afferents. Gustatory and somatic afferents from the oropharyngeal region project with a crude somatotopy within the rostral part of the NTS and visceral afferents from cardiovascular, digestive, respiratory and renal systems terminate viscero-topically within its caudal part. Moreover the NTS is extensively connected with several central structures. It projects directly to multiple brain regions by means of short connections to bulbo-ponto-mesencephalic structures (parabrachial nucleus, motor nuclei of several cranial nerves, ventro-lateral reticular formation, raphe nuclei...) and long connections to the spinal cord and diencephalic and telencephalic structures, in particular the hypothalamus and some limbic structures. The NTS is also the recipient of several central afferent inputs. It is worth to note that most of the structures that receive a direct projection from the NTS project back to the nucleus. Direct projections from the cerebral cortex to the NTS have also been identified. These extensive connections indicate that the NTS is a key structure for autonomic and neuroendocrine functions as well as for integration of somatic and autonomic responses in certain behaviors. The NTS contains a great diversity of neuroactive substances. Indeed, most of the substances identified within the central nervous system have also been detected in the NTS and may act, at this level, as classical transmitters and/or neuromodulators.(ABSTRACT TRUNCATED AT 400 WORDS)

Amino Acids↗

Gustatory responses of cortical neurons in rats. III. Neural and behavioral measures compared.

The responses of 39 cortical neurons to 13 kinds of taste stimuli including the four putative basic taste solutions (sucrose, NaCl, HCl, and quinine HCl) applied to the anterior portion of the tongue were recorded extracellularly in lightly anesthetized rats. The neural responses were analyzed in terms of the four hypotheses of quality coding: across-neuron response pattern, labeled-line, matrix pattern, and across-region response pattern notions. Animals were given a conditioned taste aversion to one of the 11 stimuli by pairing it with a gastrointestinal illness caused by intraperitoneal injection of 0.15 M LiCl. Behavioral taste profiles were constructed for each stimulus from the suppression of rate of drinking, which indicates the extent of generalization of aversion to each of the four basic taste stimuli. Neural taste profiles of each taste stimulus, which indicate the relation of the taste of a stimulus to each taste of the four basic stimuli, differed more or less depending on the kind of quality-coding notions employed. Among the four analyses, across-region correlation coefficients that were derived from an across-region response-pattern theory showed the highest correlation with the behavioral suppression rates. Therefore we conclude that processing of taste information in the cortex involves differences in both response magnitude across neurons and the spatial localization of those neurons. Fluid intake per day of each of the 12 taste solutions was measured by the single-bottle preference method. When the amount of intake was described in terms of an hedonic index (HI), which indicates the hedonic aspect of the taste of each solution, HI's for sucrose, NaCl, HCl, and quinine were 1.17, 0.43, -0.49, and -0.89, respectively. These values represent the degree of deviation of solution intake above (i.e., preferable) or below (aversive) the standard water intake. Then, HI's were calculated for each of the 12 taste stimuli based on the neural taste profiles and actual HI's for each of the four basic taste stimuli. The correlations between the calculated and the actual (or behaviorally obtained) HI's were very high (ranging from 0.832 to 0.941). This result suggests that the hedonic dimension of taste can be matched well by any one of the four proposed hypotheses.

Animals↗

Excitotoxic lesions of the gustatory thalamus spare simultaneous contrast effects but eliminate anticipatory negative contrast: evidence against a memory deficit.

Using consummately contrast procedures and the same taste stimuli (0.15% saccharin and 1.0 M sucrose), the authors tested the hypothesis that lesions of the gustatory thalamus disrupt gustatory memory in 2 experiments. In Experiment 1, irrespective of the duration of the intersolution interval (0 s, 30 s, 1 min, 2 min, 4 min, 8 min), thalamic lesions had no influence on the expression of simultaneous contrast effects. In Experiment 2, thalamic lesions abolished anticipatory negative contrast at the 0-s intersolution interval. These results provide no support for the experimental hypothesis. Rather, the data seem best interpreted as a lesion-induced disruption of the comparison mechanism responsible for anticipatory negative contrast. By this analysis, different comparison mechanisms underlie simultaneous and anticipatory contrast effects.

Affect↗

Perceptual knowledge retrieval activates sensory brain regions.

Although knowledge indexes our experiences of the world, the neural basis of this relationship remains to be determined. Previous neuroimaging research, especially involving knowledge biased to visual and functional information, suggests that semantic representations depend on modality-specific brain mechanisms. However, it is unclear whether sensory cortical regions, in general, support retrieval of perceptual knowledge. Using neuroimaging methods, we show that semantic decisions that index tactile, gustatory, auditory, and visual knowledge specifically activate brain regions associated with encoding these sensory experiences. Retrieval of tactile knowledge was specifically associated with increased activation in somatosensory, motor, and premotor cortical regions. In contrast, decisions involving flavor knowledge increased activation in an orbitofrontal region previously implicated in processing semantic comparisons among edible items. Perceptual knowledge retrieval that references visual and auditory experiences was associated with increased activity in distinct temporal brain regions involved in the respective sensory processing. These results indicate that retrieval of perceptual knowledge relies on brain regions used to mediate sensory experiences with the referenced objects.

Adolescent↗

Gustatory evoked magnetic fields in humans.

Magnetic fields evoked by taste stimuli of the human tongue were measured over the whole head using a helmet-shaped 64 channel magnetoencephalography system in five normal subjects. The stimuli were 10% glucose and 0.3 M NaCl solutions and distilled water. The most prominent peak (N175m) appearing over the bilateral hemispheres had a latency of 150-210 ms. The N175m sources were located using a two-dipole model in a spherical conducting medium based on the individual head dimensions and superimposed on magnetic resonance images. The N175m dipoles due to 10% glucose and 0.3 M NaCl stimuli were located at the operculum and circum-insular areas in both hemispheres, but those due to distilled water could not be located accurately.

Adult↗

Odor/taste integration and the perception of flavor.

Perceptions of the flavors of foods or beverages reflect information derived from multiple sensory afferents, including gustatory, olfactory, and somatosensory fibers. Although flavor perception therefore arises from the central integration of multiple sensory inputs, it is possible to distinguish the different modalities contributing to flavor, especially when attention is drawn to particular sensory characteristics. Nevertheless, our experiences of the flavor of a food or beverage are also simultaneously of an overall unitary perception. Research aimed at understanding the mechanisms behind this integrated flavor perception is, for the most part, relatively recent. However, psychophysical, neuroimaging and neurophysiological studies on cross-modal sensory interactions involved in flavor perception have started to provide an understanding of the integrated activity of sensory systems that generate such unitary perceptions, and hence the mechanisms by which these signals are "functionally united when anatomically separated". Here we review this recent research on odor/taste integration, and propose a model of flavor processing that depends on prior experience with the particular combination of sensory inputs, temporal and spatial concurrence, and attentional allocation. We propose that flavor perception depends upon neural processes occurring in chemosensory regions of the brain, including the anterior insula, frontal operculum, orbitofrontal cortex and anterior cingulate cortex, as well as upon the interaction of this chemosensory "flavor network" with other heteromodal regions including the posterior parietal cortex and possibly the ventral lateral prefrontal cortex.

Animals↗

A novel method to analyse response patterns of taste neurons by artificial neural networks.

Despite several notions on the gustatory code proposed over three decades, investigators have not yet reached a consensus. This paper describes a new approach to analyse gustatory neural activities. Three-layer neural networks were trained by the back-propagation learning algorithm, to classify the neural response patterns to four basic taste qualities. The discrimination by the trained networks on taste qualities in the response patterns of rat chorda tympani fibres (CT) and cortical taste neurons (CN) was consistent both with the correlation analysis and with behavioural experiments. By examining the connection weights of each neuron, some input neurons representing CN were 'pruned' without deteriorating the ability of the network to discriminate taste. This characteristic of the network is contrary to a previous hypothesis, that taste neurons are of equal importance in the neural coding.

Animals↗

Gustatory agnosia.

OBJECTIVE: To report the assessment of a patient exhibiting gustatory agnosia. METHODS: Preoperative and postoperative neuropsychological, neuroimaging, and chemosensory evaluations were performed in a 39-year-old woman undergoing surgical treatment for intractable epilepsy. RESULTS: Preoperative MRIs showed bilateral (right > left) atrophy in the medial temporal lobes and complete atrophy of the left insula. Evaluation of gustatory function revealed normal suprathreshold intensity estimation, affective evaluation, and detection thresholds but elevated recognition thresholds. A functional neuroimaging study showed activation to stimulation of aversive taste in the left amygdala. Surgical treatment entailed resection from the left medial temporal lobe that included the region of amygdala that had responded to taste. Postoperatively, detection, naming, and intensity estimation for taste remained normal, but the patient was unable to recognize different tastes (sweet, sour, salty, and bitter). A second evaluation 2.5 years after her surgery revealed no change in taste ability. CONCLUSION: The anteromedial temporal lobe has an important role in recognizing taste quality.

Adult↗

Response properties of neurons to sucrose in the reward phase and the areal distribution in the monkey fronto-operculuro-insular and prefrontal cortices during a taste discrimination GO/NOGO task.

The neural activities to sucrose in the reward phase were examined in the primate fronto-operculo-insular and prefrontal cortices during a NaCl-water discrimination GO/NOGO task. Neurons were classified according to the cue-responsiveness into sucrose-specific, cue-differential, or cue-non-differential groups. The onset latencies and decay times divided response temporal patterns into four types. All cue-non-differential neurons were the short latency-short decay type, whereas most sucrose-specific and cue-differential neurons were either the short latency-short decay or short latency-long decay type. Most neurons were histologically located in areas G, 3, and 1-2, the primary gustatory cortices (PGCs), and the precentral operculum, one of the higher-order gustatory cortices (HGCs), whereas a few were in other HGCs, e.g., area 12. Further study of the temporal properties of the neurons in each cortical area revealed two subgroups of short-latency responses with different onset latencies and a group of responses with an intermediate decay time around the boundary between short- and long-decay times in the PGCs. The onset latencies to cues and sucrose were significantly correlated in the HGC, but not in the PGC. These results indicate that different processing mechanisms operate for sucrose in the reward phase in the PGC and HGC.

Action Potentials↗