Tullio Manzoni

Posterior Corpus Callosum and Interhemispheric Transfer of Somatosensory Information: An fMRI and Neuropsychological Study of a Partially Callosotomized Patient

Interhemispheric somatosensory transfer was studied by functional magnetic resonance imaging (fMRI) and neuropsychological tests in a patient who underwent resection of the corpus callosum (CC) for drug-resistant epilepsy in two stages. The first resection involved the anterior half of the body of CC and the second, its posterior half and the splenium. For the fMRI study, the hand was stimulated with a rough sponge. The neuropsychological tests included: Tactile Naming Test (TNT), Same-Different Recognition Test (SDRT), and Tactile Finger Localization Test (intra- and intermanual tasks, TFLT). The patient was studied 1 week before and then 6 months and 1 year after the second surgery. Before this operation, unilateral tactile stimulation of either hand activated contralaterally the first (SI) and second (SII) somatosensory areas and the posterior parietal (PP) cortex, and SII and PP cortex ipsilaterally. All three tests were performed without errors. In both postoperative sessions, somatosensory activation was observed in contralateral SI, SII, and PP cortex, but not in ipsilateral SII and PP cortex. Performance was 100 correct in the TNT for the right hand, but below chance for the left; in the other tests, it was below chance except for TFLT in the intramanual task. This case provides the direct demonstration that activation of SII and PP cortex to stimulation of the ipsilateral hand and normal interhemispheric transfer of tactile information require the integrity of the posterior body of the CC.

Callosal mechanism for the interhemispheric transfer of hand somatosensory information in the monkey.

The retrograde transport of horseradish peroxidase (HRP) was combined with extracellular microelectrode recording from single and multiple-neurones to study the anatomical and functional organization of the callosal connections of the hand sensory projection field in the parietal operculum of monkeys (Macaca Irus). In 3 animals anaesthetized with ketamine, a single injection of HRP (0.5 microliter) was delivered into the cortex forming the upper bank of the sylvian sulcus at a site where neuronal responses to somatic sensory stimulation of the hand were recorded. In the ipsilateral hemisphere, retrogradely HRP-labelled cells were found in the cortex of the post-central gyrus and in the thalamic nuclei ventralis posteroinferior and pulvinar oralis. In the contralateral hemisphere HRP-labelled neurones were present in the opercular cortex lying dorsal, and slightly caudal, to the posterior pole of the insula. Few scattered callosal neurones were also found in the post-central gyrus. In 3 other animals, multiple injections (5-8; 0.5 microliter each) of HRP were performed in the parietal operculum. In the ipsilateral hemisphere, retrogradely labelled cells were present in the post-central gyrus and in the following thalamic nuclei: ventralis posteroinferior, pulvinar oralis and medialis, ventralis posteromedialis and posterior complex. Few labelled cells were also present in the ventral part of the nucleus ventralis posterolateralis. In the contralateral hemisphere, numerous callosal cells were labelled with HRP. These cells were found, with regional variations in density, in wide regions of the buried and exposed cortex of the parietal operculum and in the post-central gyrus. These 3 monkeys were subjected to microelectrode mapping experiments (N2O and halothane anaesthesia) to explore the peripheral receptive fields of neurones in the parietal operculum and post-central gyrus contralateral to the injected side. HRP labelled callosal neurones were found in regions of the second and first somatosensory cortical areas which also contained units driven from the contralateral hand.

Demonstration of glutamate-positive axon terminals forming asymmetric synapses in cat neocortex

Electron microscopic examination of sections immunocytochemically processed with an anti-glutamate serum reveals that many asymmetric synapses in the cat neocortex contain elevated levels of immunodetectable glutamate. These labelled axon terminals are likely to use glutamate as neurotransmitter. Axon terminals forming symmetric contacts were never labelled. Since glutamate is known to exert potent excitatory effects on neocortical neurons, the present finding gives immunocytochemical evidence that asymmetric synapses are excitatory.

Role of the corpus callosum in the somatosensory activation of the ipsilateral cerebral cortex: an fMRI study of callosotomized patients

To verify whether the activation of the posterior parietal and parietal opercular cortices to tactile stimulation of the ipsilateral hand is mediated by the corpus callosum, a functional magnetic resonance imaging (fMRI, 1.0 tesla) study was performed in 12 control and 12 callosotomized subjects (three with total and nine with partial resection). Eleven patients were also submitted to the tactile naming test. In all subjects, unilateral tactile stimulation provoked a signal increase temporally correlated with the stimulus in three cortical regions of the contralateral hemisphere. One corresponded to the first somatosensory area, the second was in the posterior parietal cortex, and the third in the parietal opercular cortex. In controls, activation was also observed in the ipsilateral posterior parietal and parietal opercular cortices, in regions anatomically corresponding to those activated contralaterally. In callosotomized subjects, activation in the ipsilateral hemisphere was observed only in two patients with splenium and posterior body intact. These two patients and another four with the entire splenium and variable portions of the posterior body unsectioned named objects explored with the right and left hand without errors. This ability was impaired in the other patients. The present physiological and anatomical data indicate that in humans activation of the posterior parietal and parietal opercular cortices in the hemisphere ipsilateral to the stimulated hand is mediated by the corpus callosum, and that the commissural fibres involved probably cross the midline in the posterior third of its body.

Topographical organization of human corpus callosum: An fMRI mapping study

The concept of a topographical map of the corpus callosum (CC) has emerged from human lesion studies and from anatomical tracing investigations in other mammals. Over the last few years, a rising number of researchers have been reporting functional magnetic resonance imaging (fMRI) activation in white matter, particularly the CC. In this study, the scope for describing CC topography with fMRI was explored by evoking activation through simple sensory stimulation and motor tasks. We reviewed our published and unpublished fMRI data on the cortical representation of tactile, gustatory, and visual sensitivity and of motor activation, obtained in 36 volunteers. Activation foci were consistently detected in discrete CC regions: anterior (taste stimuli), central (motor tasks), central and posterior (tactile stimuli), and splenium (visual stimuli). These findings demonstrate that the functional topography of the CC can be explored with fMRI.

Postnatal development of the glutamate vesicular transporter VGLUT1 in rat cerebral cortex

The expression of the vesicular glutamate transporter VGLUT1 in the rat neocortex was studied during postnatal development using immunocytochemistry and Western blotting. At all ages, VGLUT immunoreactivity is localized to puncta that coexpress the presynaptic marker synaptophysin. VGLUT1 immunoreactivity is faint at birth, increases in the subplate during the first postnatal week, invades the supragranular layers in the second week and reaches the adult pattern at P20-P30. Its spatial and temporal maturation patterns suggest that VGLUT1 may be the vesicular transporter in developing corticocortical connections.

Bilateral Receptive Fields and Callosal Connectivity of the Body Midline Representation in the First Somatosensory Area of Primates

Experiments were performed in order to study the receptive field (RF) organization and the callosal connectivity of the trunk representation zone in areas 3b and 1 of the postcentral cortex of macaque monkeys. Multiunit microelectrode recordings showed that neurons responding to tactile stimulation of bilateral RFs across the midline of the body were contained in three topographically distinct zones of the trunk map. In one zone, at the junction between cytoarchitectonic areas 3b and 1, RFs straddled the dorsal midline of the trunk. In the other two zones, one located caudally in area 1 in front of the postcentral dimple, and the other rostrally in area 3b in the depth of the posterior bank of the central sulcus, RFs straddled the ventral midline of the trunk. The first one and the other two zones are referred to here as the dorsal and the ventral midline representation zones, respectively. Elsewhere in the trunk map, neurons responded only to stimulation of contralateral RFs. The callosal connectivity of the trunk map was studied by means of the transport of horseradish peroxidase (HRP). Multiple injections of HRP in electrophysiologically identified sites of the trunk representation in one hemisphere labeled both callosal fiber terminals and callosally projecting neurons in the contralateral homotopic cortex. Dense patches of callosal neurons intensely labeled with HRP were present in the cortical regions representing the body midlines and were distributed for the most part in layer III. Some neurons lightly labeled with HRP were scattered in other zones of the trunk map. Callosal terminations were densest within the midline zones and very sparse or absent in the lateral trunk zones. Correlation of physiological and anatomical data obtained either separately or from the same animal demonstrated that cortical regions containing bilateral-field neurons also contained the highest density of labeled callosal terminations and neurons. This correlation suggests a role for the corpus callosum in the perception of the body midline, either by generating the bilateral RFs of these neurons or by coordinating the activity of the regions containing neurons with thalamically generated bilateral RFs.

Immunocytochemical evidence for glutamatergic cortico-cortical connections in monkeys.

Retrograde transport of horseradish peroxidase and immunocytochemical visualization of glutamate (Glu) were combined to investigate the neurotransmitter used by cortico-cortical neurons in the first (SI) and second (SII) somatic sensory areas of macaque monkeys. The majority of association and callosal neurons in SI and SII were immunoreactive for an antiGlu serum: evidence was therefore obtained in support of a role for Glu, or a closely related compound, as the synaptic transmitter used by cortico-cortical fibers.

Bilateral cortical representation of the trunk midline in human first somatic sensory area

The cortical representation of the trunk zone in the human first somatosensory area was studied with functional magnetic resonance imaging (fMRI) to establish whether the cutaneous regions close to the midline are represented in this area of both hemispheres. Cortical activation foci evoked by unilateral tactile stimulation of ventral trunk regions were detected in the postcentral gyrus of the contralateral hemisphere slightly medial to or just behind the omega‐shaped region of the central sulcus and in the anterior bank of the postcentral sulcus. These regions probably correspond to the trunk ventral midline representation zones of areas 3a–3b and 1–2, respectively. Stimulation of cutaneous regions adjacent to the midline evoked activation foci also in the ipsilateral postcentral gyrus in regions symmetrical to those activated in the contralateral hemisphere. These data demonstrate that in humans, as in nonhuman primates, the cutaneous regions adjacent to the trunk midline are represented bilaterally in the first somatic sensory cortex. Whether the ipsilateral activation depends on callosal or extracallosal inputs remains to be elucidated. Hum Brain Mapping, 2005.

Taste laterality in the split brain

Two patients with corpus callosum resection, one complete and the other sparing the genu and the rostrum, were tested for discrimination of three basic taste stimuli (sour, bitter, salty) applied to the right or left sides of the tongue. Responses were made by pointing with either hand to written words or images of visual objects corresponding to the stimuli, a language‐based discrimination. In both patients, response accuracy was significantly above chance for both hemitongues but there was a significant advantage for the left side. Reaction time was shorter for left stimuli than for right stimuli but the difference was not significant. Eight normal controls matched for age with the patients performed equally well with right and left hemitongue stimuli and so did a third callosotomy patient with sparing of the posterior callosum, including the splenium. Tactile and visual tests showed that the left hemisphere was responsible for language‐based responses in the first two patients. The results confirm and extend previous findings in another callosotomy patient, indicating that: (i) taste information from either side of the tongue can reach the left hemisphere in the absence of the corpus callosum; (ii) the ipsilateral input from the tongue to the left hemisphere is more potent functionally than the contralateral input and (iii) in the normal brain, the corpus callosum, specifically its posterior part including the splenium, appears to equalize the effects of the ipsilateral and contralateral gustatory inputs on the left hemisphere. Taken together with evidence about lateralized taste deficits following unilateral cortical lesions, the results also suggest that the gustatory pathways from tongue to cortex are bilaterally‐distributed with an ipsilateral predominance that may be subject to individual variations.