Modality-specific neural effects of selective attention to taste and odor

The insular cortex is implicated in general attention and in taste perception. The effect of selective attention to taste on insular responses may therefore reflect a general effect of attention or it may be (taste) modality specific. To distinguish between these 2 possibilities, we used functional magnetic resonance imaging to evaluate brain response to tastes and odors while subjects passively sampled the stimuli or performed a detection task. We found that trying to detect a taste (attention to taste) resulted in activation of the primary taste cortex (anterior and mid-dorsal insula) but not in the primary olfactory cortex (piriform). In contrast, trying to detect an odor (attention to odor) increased activity in primary olfactory but not primary gustatory cortex. However, we did identify a region of far anterior insular cortex that responded to both taste and odor "searches." These results demonstrate modality-specific activation of primary taste cortex by attention to taste and primary olfactory cortex by attention to odor and rule out the possibility that either response reflects a general effect of attentional deployment. The findings also support the existence of a multimodal region in far anterior insular cortex that is sensitive to directed attention to taste and smell.     

Somatosensory evoked potentials following lesions of the claustrum

Ipsi- and contralateral cortical somatosensory evoked potentials (SEP) were recorded following median nerve stimulation in 12 patients with unilateral brain lesions and in 5 healthy subjects. Computed tomographic scans of brain were performed on admission. In all patients with lesions of the claustrum there was absence of SEP contralateral to the side of the lesion and ipsilateral to the stimulated nerve. This phenomenon did not appear in our material following lesions involving other structures e.g. thalamus or somatosensory cortex. Our observations suggest that the claustrum may influence deeply the contralateral somatosensory cortex. This may be due to the fact that a large part of the claustrum is involved in transmission of the sensory information from receptors to the somatosensory cortex.     

Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry.

A working hypothesis is proposed for piriform cortex (PC) and other olfactory cortical areas that redefines the traditional functional roles as follows: the olfactory bulb serves as the primary olfactory cortex by virtue of encoding 'molecular features' (structural components common to many odorant molecules) as a patchy mosaic reminiscent of the representation of simple features in primary visual cortex. The anterior olfactory cortex (that has been inappropriately termed the anterior olfactory nucleus) detects and stores correlations between olfactory features, creating representations (gestalts) for particular odorants and odorant mixtures. This function places anterior olfactory cortex at the level of secondary visual cortex. PC carries out functions that have traditionally defined association cortex--it detects and learns correlations between olfactory gestalts formed in anterior olfactory cortex and a large repertoire of behavioral, cognitive and contextual information to which it has access through reciprocal connections with prefrontal, entorhinal, perirhinal and amygdaloid areas. Using principles derived from artificial networks with biologically plausible parallel-distributed architectures and Hebbian synaptic plasticity (i.e. adjustments in synaptic strength based on locally convergent activity), functional proposals are made for PC and related cortical areas. Architectural features incorporated include extensive recurrent connectivity in anterior PC, predominantly feedforward connectivity in posterior PC and backprojections that connect distal to proximal structures in the cascade of olfactory cortical areas. Capabilities of the 'reciprocal feedforward correlation' architecture that characterizes PC and adjoining higher-order areas are discussed in some detail. The working hypothesis is preceded by a review of relevant anatomy and physiology, and a non-quantitative account of parallel-distributed principles. To increase the accessibility of findings for PC and to advertise its substantial potential as a model for experimental and modeling analysis of associative processes, parallels are described between PC and the hippocampal formation, inferotemporal visual cortex and prefrontal cortex.     

Physiology and morphology of protocerebral olfactory neurons in the male moth Manduca sexta

1. We have used intracellular recording and staining with Lucifer Yellow, followed by reconstruction from serial sections, to characterize the responses and structure of olfactory neurons in the protocerebrum (PC) of the brain of the male sphinx moth Manduca sexta. 2. Many olfactory protocerebral neurons (PCNs) innervate a particular neuropil region lateral to the central body, the lateral accessory lobe (LAL), which appears to be important for processing olfactory information. 3. Each LAL is linked by its constituent neurons to the ipsilateral lateral PC, where projection neurons from the antennal lobe terminate, as well as to other regions of the PC. The LALs are also linked to each other by bilateral neurons with arborizations in each LAL. 4. Some PC neurons showed long-lasting excitation (LLE) that outlasted the olfactory stimuli by greater than or equal to 1 s, and as long as 30 s in some preparations. LLE was more frequently elicited by the sex-pheromone blend than by individual pheromone components. All bilateral neurons that showed LLE had arborizations in the LALs. LLE responses were also recorded in a single local neuron innervating the mushroom body. 5. In some other PC neurons, pheromonal stimuli elicited brief excitations that recovered to background firing rates less than 1 s after stimulation.     

fMRI activation in response to odorants orally delivered in aqueous solutions

During food intake flavor perception results from simultaneous stimulation of the gustatory, olfactory and trigeminal systems. Olfactory stimulation occurs mainly through the retronasal pathway and the resulting perception is often interpreted as a taste perception, thus leading to the well-known sensory confusion between taste and olfaction. The present experiment was designed to study, with functional magnetic resonance imaging (fMRI), the cortical representation of olfactory perception in humans in response to retronasal stimulation by odorants delivered in aqueous solution. Psychophysical evaluation confirmed that the stimuli acted as pure olfactory stimuli through the retronasal pathway and did not present any taste component. Results showed activation in all brain regions previously described with neuroimaging techniques using olfactory stimulation with an odorized air flow. Piriform and orbitofrontal cortex were found activated as well as the hippocampal region, the amygdala, the insular lobe, the cingulate gyrus and the cerebellum. These results demonstrate the feasibility of efficiently stimulating the olfactory system in an fMRI scanner through the retronasal pathway with liquids delivered to the oral cavity. The presentation of olfactory stimuli in liquids to the mouth is a realistic model for the study of food-related flavor perception. This stimulation protocol furthermore allows presenting taste and olfactory stimuli separately or combined, thus allowing for direct comparisons between single modality representation, taste or olfaction, and representation of multi-modality mixtures.     

Spatiotemporal properties of the action potential propagation in the mouse visual cortical slice analyzed by calcium imaging

The calcium ion (Ca(2+)) is an important messenger for signal transduction, and the intracellular Ca(2+) concentration ([Ca(2+)](i)) changes in response to an excitation of the cell. To reveal the spatiotemporal properties of the propagation of an excitatory signal with action potentials in the primary visual cortical circuit, we conducted a Ca(2+) imaging study on slices of the mouse visual cortex. Electrical stimulation of layer 4 evoked [Ca(2+)](i) transients around the stimulus electrode. Subsequently, the high [Ca(2+)](i) region mainly propagated perpendicular to the cortical layer (vertical propagation), with horizontal propagation being restricted. When the excitatory synaptic transmission was blocked, only weak and concentric [Ca(2+)](i) transients were observed. When the action potential was blocked, the [Ca(2+)](i) transients disappeared almost completely. These results suggested that the action potential contributed to the induction of the [Ca(2+)](i) transients, and that excitatory synaptic connections were involved in the propagation of the high [Ca(2+)](i) region in the primary visual cortical circuit. To elucidate the involvement of inhibitory synaptic connections in signal propagation in the primary visual cortex, the GABA(A) receptor inhibitor bicuculline was applied. In this case, the evoked signal propagated from layer 4 to the entire field of view, and the prolonged [Ca(2+)](i) transients were observed compared with the control condition. Our results suggest that excitatory neurons are widely connected to each other over the entire primary visual cortex with recurrent synapses, and inhibitory neurons play a fundamental role in the organization of functional sub-networks by restricting the propagation of excitation signals.     

Extensive Lesions in Rat Insular Cortex Significantly Disrupt Taste Sensitivity to NaCl and KCl and Slow Salt Discrimination Learning

While studies of the gustatory cortex (GC) mostly focus on its role in taste aversion learning and memory, the necessity of GC for other fundamental taste-guided behaviors remains largely untested. Here, rats with either excitotoxic lesions targeting GC (n = 26) or sham lesions (n = 14) were assessed for postsurgical retention of a presurgically LiCl-induced conditioned taste aversion (CTA) to 0.1M sucrose using a brief-access taste generalization test in a gustometer. The same animals were then trained in a two-response operant taste detection task and psychophysically tested for their salt (NaCl or KCl) sensitivity. Next, the rats were trained and tested in a NaCl vs. KCl taste discrimination task with concentrations varied. Rats meeting our histological inclusion criterion had large lesions (resulting in a group averaging 80% damage to GC and involving surrounding regions) and showed impaired postsurgical expression of the presurgical CTA (LiCl-injected, n = 9), demonstrated rightward shifts in the NaCl (0.54 log₁₀ shift) and KCl (0.35 log₁₀ shift) psychometric functions, and displayed retarded salt discrimination acquisition (n = 18), but eventually learned and performed the discrimination comparable to sham-operated animals. Interestingly, the degree of deficit between tasks correlated only modestly, if at all, suggesting that idiosyncratic differences in insular cortex lesion topography were the root of the individual differences in the behavioral effects demonstrated here. This latter finding hints at some degree of interanimal variation in the functional topography of insular cortex. Overall, GC appears to be necessary to maintain normal taste sensitivity to NaCl and KCl and for salt discrimination learning. However, higher salt concentrations can be detected and discriminated by rats with extensive damage to GC suggesting that the other resources of the gustatory system are sufficient to maintain partial competence in these tasks, supporting the view that such basic sensory-discriminative taste functions involve distributed processes among central gustatory structures.     

Diversity of spatial relationships of the claustrum and insula in branches of the mammalian radiation

Using digital images of stained sections, we conducted a comparative survey of the visible gross morphology of the insular cortex and the claustrum in 26 mammalian species, representing most of the major mammalian radiations. We observed several features that are conserved in the mammals that we examined, including the absence of expansion of the insular cortex into out-branching lobes, the adherence of the claustrum to the fundus of the rhinal sulcus and to endopiriform cellular regions, and several features that varied, including the colocation of the insular and claustrocortex, the cortical origin of the operculations that cover the insula, the locations of large accumulations of claustral cells, and the presence of thin extensions of groups of claustral cells. We suggest that the final shape of the claustrum is highly influenced by the expansion of two medially adjacent subcortical structures, the striatum and amygdala. We further suggest that the neighboring locations of the claustrum and insula may be due to a dependence of each of these structures upon proximity to olfactory cortex, rather than to any connectional relationships between them.     

The claustrum in the dog brain.

The structure of the claustrum was studied in the dog brain using Weigert's, Klüver-Barrera's, Manns' and Nissl's methods. It consists of two main parts arranged one above the other. The dorsal part is situated in the depth of the neocortex and extends from the gyrus orbitalis to the gyrus compositus posterior. The ventral part of the claustrum underlying the olfactory cortex continues from the cuadal fragments of the olfactory peduncle to the entorhinal area, where it fuses with its deep layers. The claustrum can be regarded as a fragment of a bigger cellular formation present in different parts of the hemisphere.     

The effect of food odor background on gustatory preferences and gustatory behavior of carp <Emphasis Type="Italic">Cyprinus carpio</Emphasis> and cod <Emphasis Type="Italic">Gadus morhua</Emphasis>

It was shown that stimulation by food odor (aquatic extract of food organisms, 10^?2 and 10^?3 g/l) does not cause shifts in gustatory preferences in carp Cyprinus carpio and cod Gadus morhua but modifies gustatory behavior. The level of consumption by carp of control granules and granules with attractive, by taste, L-proline (0.1 M) or deterrent L-lysine (0.1 M) (item by item presentation of granules) and by cod of control granules and granules with indifferent, to it, L-asparagine (0.1 M) (presentation of 10 granules simultaneously) is similar prior to and during olfactory stimulation. In the presence of food odor, the duration of taste testing for most types of granules, as well as the number of repeated graspings of granules with an attractive taste do not change in fish. At the same time, granules with indifferent or repulsive gustatory properties are rejected and repeatedly grasped by fish against the background of food odor more frequently than in water without odor. Olfactory stimulation leads to a considerable increase in the average number of graspings per one grasped granule with an indifferent or repulsive taste. Such behavior manifested by fish in the presence of food odor in response to granules with unattractive gustatory properties is apparently caused by the contradiction between the information coming via different chemosensory canals—olfactory and gustatory. The obtained results indicate that food stimulation caused by food odor in nature can lead to an increase in the actual consumption of only those accessible food items that have an attractive taste for fish.     

State-dependent sensory gating in olfactory cortex

Sensory systems show behavioral state-dependent gating of information flow that largely depends on the thalamus. Here we examined whether the state-dependent gating occurs in the central olfactory pathway that lacks a thalamic relay. In urethane-anesthetized rats, neocortical EEG showed a periodical alternation between two states: a slow-wave state (SWS) characterized by large and slow waves and a fast-wave state (FWS) characterized by faster waves. Single-unit recordings from olfactory cortex neurons showed robust spike responses to adequate odorants during FWS, whereas they showed only weak responses during SWS. The state-dependent change in odorant-evoked responses was observed in a majority of olfactory cortex neurons, but in only a small percentage of olfactory bulb neurons. These findings demonstrate a powerful state-dependent gating of odor information in the olfactory cortex that works in synchrony with the gating of other sensory systems. They suggest a state-dependent switchover of signal processing modes in the olfactory cortex.     

Neural processing of gustatory information in insular circuits

The insular cortex is the primary cortical site devoted to taste processing. A large body of evidence is available for how insular neurons respond to gustatory stimulation in both anesthetized and behaving animals. Most of the reports describe broadly tuned neurons that are involved in processing the chemosensory, physiological and psychological aspects of gustatory experience. However little is known about how these neural responses map onto insular circuits. Particularly mysterious is the functional role of the three subdivisions of the insular cortex: the granular, the dysgranular and the agranular insular cortices. In this article we review data on the organization of the local and long-distance circuits in the three subdivisions. The functional significance of these results is discussed in light of the latest electrophysiological data. A view of the insular cortex as a functionally integrated system devoted to processing gustatory, multimodal, cognitive and affective information is proposed.     

Cerebral activation to intranasal chemosensory trigeminal stimulation

Although numerous functional magnetic resonance imaging (FMRI) studies have been performed on the processing of olfactory information, the intranasal trigeminal system so far has not received much attention. In the present study, we sought to delineate the neural correlates of trigeminal stimulation using carbon dioxide (CO(2)) presented to the left or right nostril. Fifteen right-handed men underwent FMRI using single runs of 3 conditions (CO(2) in the right and the left nostrils and an olfactory stimulant-phenyl ethyl alcohol-in the right nostril). As expected, olfactory activations were located in the orbitofrontal cortex (OFC), amygdala, and rostral insula. For trigeminal stimulation, activations were found in "trigeminal" and "olfactory" regions including the pre- and postcentral gyrus, the cerebellum, the ventrolateral thalamus, the insula, the contralateral piriform cortex, and the OFC. Left compared with right side stimulations resulted in stronger cerebellar and brain stem activations; right versus left stimulation resulted in stronger activations of the superior temporal sulcus and OFC. These results suggest a trigeminal processing system that taps into similar cortical regions and yet is separate from that of the olfactory system. The overlapping pattern of cortical activation for trigeminal and olfactory stimuli is assumed to be due to the intimate connections in the processing of information from the 2 major intranasal chemosensory systems.     

Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception

Nitric oxide (NO) modulates the dynamics of central olfactory networks and has been implicated in olfactory processing including learning. Land mollusks have a specialized olfactory lobe in the brain called the procerebral (PC) lobe. The PC lobe produces ongoing local field potential (LFP) oscillation, which is modulated by olfactory stimulation. We hypothesized that NO should be released in the PC lobe in response to olfactory stimulation, and to prove this, we applied an NO electrode to the PC lobe of the land slug Limax in an isolated tentacle-brain preparation. Olfactory stimulation applied to the olfactory epithelium transiently increased the NO concentration in the PC lobe, and this was blocked by the NO synthase inhibitor L-NAME at 3.7 mM. L-NAME at this concentration did not block the ongoing LFP oscillation, but did block the frequency increase during olfactory stimulation. Olfactory stimulation also enhanced spatial synchronicity of activity, and this response was also blocked by L-NAME. Single electrical stimulation of the superior tentacle nerve (STN) mimicked the effects of olfactory stimulation on LFP frequency and synchronicity, and both of these effects were blocked by L-NAME. L-NAME did not block synaptic transmission from the STN to the nonbursting (NB)-type PC lobe neurons, which presumably produce NO in an activity-dependent manner. Previous behavioral experiments have revealed impairment of olfactory discrimination after L-NAME injection. The recording conditions in the present work likely reproduce the in vivo brain state in those behavioral experiments. We speculate that the dynamical effects of NO released during olfactory perception underlie precise odor representation and memory formation in the brain, presumably through regulation of NB neuron activity.     

GABAergic modulation of primary gustatory afferent synaptic efficacy

Modulation of synaptic transmission at the primary sensory afferent synapse is well documented for the somatosensory and olfactory systems. The present study was undertaken to test whether GABA impacts on transmission of gustatory information at the primary afferent synapse. In goldfish, the vagal gustatory input terminates in a laminated structure, the vagal lobes, whose sensory layers are homologous to the mammalian nucleus of the solitary tract. We relied on immunoreactivity for the GABA-transporter, GAT-1, to determine the distribution of GABAergic synapses in the vagal lobe. Immunocytochemistry showed dense, punctate GAT-1 immunoreactivity coincident with the layers of termination of primary afferent fibers. The laminar nature and polarized dendritic structure of the vagal lobe make it amenable to an in vitro slice preparation to study early synaptic events in the transmission of gustatory input. Electrical stimulation of the gustatory nerves in vitro produces synaptic field potentials (fEPSPs) predominantly mediated by ionotropic glutamate receptors. Bath application of either the GABA(A) receptor agonist muscimol or the GABA(B) receptor agonist baclofen caused a nearly complete suppression of the primary fEPSP. Coapplication of the appropriate GABA(A) or GABA(B) receptor antagonist bicuculline or CGP-55845 significantly reversed the effects of the agonists. These data indicate that GABAergic terminals situated in proximity to primary gustatory afferent terminals can modulate primary afferent input via both GABA(A) and GABA(B) receptors. The mechanism of action of GABA(B) receptors suggests a presynaptic locus of action for that receptor.     

Topography of Gng2- and NetrinG2-Expression Suggests an Insular Origin of the Human Claustrum

The claustrum has been described in the forebrain of all mammals studied so far. It has been suggested that the claustrum plays a role in the integration of multisensory information: however, its detailed structure and function remain enigmatic. The human claustrum is a thin, irregular, sheet of grey matter located between the inner surface of the insular cortex and the outer surface of the putamen. Recently, the G-protein gamma2 subunit (Gng2) was proposed as a specific claustrum marker in the rat, and used to better delineate its anatomical boundaries and connections. Additional claustral markers proposed in mammals include Netrin-G2 in the monkey and latexin in the cat. Here we report the expression and distribution of Gng2 and Netrin-G2 in human post-mortem samples of the claustrum and adjacent structures. Gng2 immunoreactivity was detected in the neuropil of the claustrum and of the insular cortex but not in the putamen. A faint labelling was present also in the external and extreme capsules. Double-labelling experiments indicate that Gng2 is also expressed in glial cells. Netrin-G2 labelling was seen in neuronal cell bodies throughout the claustrum and the insular cortex but not in the medially adjacent putamen. No latexin immunoreactive element was detected in the claustrum or adjacent structures. Our results confirm that both the Gng2 and the Netrin-G2 proteins show an affinity to the claustrum and related formations also in the human brain. The presence of Gng2 and Netrin-G2 immunoreactive elements in the insular cortex, but not in the putamen, suggests a possible common ontogeny of the claustrum and insula.     

Functional aspects of the relation between the claustrum and motor cortex in the cat

In order to study the relationships between the claustrum and motor cortex neurons both of area 4 and area 6 in the cat, an experiment was performed in which the effect of claustral stimulation on pyramidal tract neurons was investigated. Single shock electrical activation of the claustrum caused an inhibition of the spontaneous activity of the neurons, or an inhibition preceded by short activation, or no effect. These evidences lead to the conclusion that the claustrum exerts a role in movement organization.     

Some introductory notes on the organization of the forebrain in tetrapods.

As an introduction to the main theme of this conference an overview of the organization of the tetrapod forebrain is presented with emphasis on the telencephalic representation of sensory and motor functions. In all classes of tetrapods, olfactory, visual, octavolateral, somatosensory and gustatory information reaches the telencephalon. Major differences exist in the telencephalic targets of sensory information between amphibians and amniotes. In amphibians, three targets are found: the lateral pallium for olfactory input, the medial pallium for visual and multisensory input, and the lateral subpallium for visual, octavolateral and somatosensory information. The forebrains of reptiles and mammals are similar in that the dorsal surface of their cerebral hemisphere is formed by a pallium with three major segments: (a) an olfactory, lateral cortex; (b) a 'limbic' cortex that forms the dorsomedial wall of the hemisphere, and (c) an intermediate cortex that is composed entirely of isocortex in mammals, but in reptiles (and birds) consists of at least part of the dorsal cortex (in birds the Wulst) and a large intraventricular protrusion, i.e. the dorsal ventricular ridge. In birds, the entire lateral wall of the hemisphere is involved in this expansion. The intermediate pallial segment receives sensory projections from the thalamus and contains modality-specific sensory areas in reptiles, birds and mammals. The most important differences between the intermediate pallial segment of amniotes concern motor systems.     

Long-term modifications in the strength of excitatory associative inputs in the piriform cortex

Afferent olfactory information, in vivo and in vitro, can be rapidly adapted to through a metabotropic glutamate receptor (mGluR)-mediated attenuation of synaptic strength. Specific cellular and synaptic mechanisms underlying olfactory learning and habituation at the cortical level remain unclear. Through whole-cell recording, excitatory postsynaptic currents (EPSCs) were obtained from piriform cortex (PC) principal cells. Using a coincidental, pre- and postsynaptic stimulation protocol, long-term depression (LTD) in synaptic strength was induced at associative, excitatory synapses onto layer II pyramidal neurons of the mouse (P15-27) PC. LTD was mimicked and occluded by mGluR agonists and blocked by nonselective mGluR antagonist (RS)-alpha-methyl-4-sulfonophenylglycine (MSPG) but not by N-methyl-D-aspartic acid (NMDA) receptor antagonist 2-amino-5-phosphonovaleric acid (APV). Analysis of the paired-pulse ratio, alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/NMDA current ratio, and spontaneous EPSCs indicate that electrically induced LTD was mediated predominantly by postsynaptic mechanisms. Additionally, presynaptic mGluRs were involved in agonist-mediated synaptic depression. Immunohistochemical analysis supports the presence of multiple subclasses of mGluRs throughout the PC, with large concentrations of several receptors present in layer II. These observations provide further evidence of activity-dependent, long-term modification of associative inputs and its underlying mechanisms. Cortical adaptation at associative synapses provides an additional link between cortical olfactory processing and subcortical centers that influence behavior.