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Jon H Kaas

Publications and source records attributed to Jon H Kaas.

At least 19 recordsLinked to original sources

The organization of frontoparietal cortex in the tree shrew (Tupaia belangeri): II. Connectional evidence for a frontal-posterior parietal network.

Tree shrews are small squirrel-like mammals that are the closest living relative to primates available for detailed neurobiological study. In a recent study (Remple et al. [2006] J. Comp. Neurol. 497:133-154), we provided anatomical and electrophysiological evidence that the frontoparietal cortex of tree shrews has two motor fields (M1 and M2) and five somatosensory fields (3a, 3b, S2, somatosensory caudal area [SC], and parietal ventral area [PV]). In the present study, we injected anatomical tracers into M1, M2, 3a, 3b, SC, and posterior parietal cortex to establish the ipsilateral cortical connections of these areas. The results provide evidence for a number of new cortical areas including medial motor and somatosensory areas (MMA and MSA), three posterior parietal areas (PPd, PPv, and PPc), and an area ventral to temporal inferior cortex (TIV). Ml receives topographic projections from M2, MMA, 3a, and PPv, and nontopographic connections from the temporal anterior and dorsal areas (TA and TD), PPc, TIV, and MSA. The connections of M2 are similar to those of M1, except that M2 receives denser projections from TIV, PPc, and dorsal frontal cortex and sparser input from M1. Areas 3a, 3b, and SC receive dense topographic projections from each other, S2, and PV and sparser connections from PPd and PPv. Area 3a receives additional input from posterior parietal and temporal regions and from M1 and MMA. Overall, the frontoparietal connections of tree shrew cortex are most similar to those of prosimian primates and quite different from those of more distant relatives such as rats.

Animals↗

Cortical and thalamic connections of the representations of the teeth and tongue in somatosensory cortex of new world monkeys.

Connections of representations of the teeth and tongue in primary somatosensory cortex (area 3b) and adjoining cortex were revealed in owl, squirrel, and marmoset monkeys with injections of fluorescent tracers. Injection sites were identified by microelectrode recordings from neurons responsive to touch on the teeth or tongue. Patterns of cortical label were related to myeloarchitecture in sections cut parallel to the surface of flattened cortex, and to coronal sections of the thalamus processed for cytochrome oxidase (CO). Cortical sections revealed a caudorostral series of myelin dense ovals (O1-O4) in area 3b that represent the periodontal receptors of the contralateral teeth, the contralateral tongue, the ipsilateral teeth, and the ipsilateral tongue. The ventroposterior medial subnucleus, VPM, and the ventroposterior medial parvicellular nucleus for taste, VPMpc, were identified in the thalamic sections. Injections placed in the O1 oval representing teeth labeled neurons in VPM, while injections in O2 representing the tongue labeled neurons in both VPMpc and VPM. These injections also labeled adjacent part of areas 3a and 1, and locations in the lateral sulcus and frontal lobe. Callosally, connections of the ovals were most dense with corresponding ovals. Injections in the area 1 representation of the tongue labeled neurons in VPMpc and VPM, and ipsilateral area 3b ovals, area 3a, opercular cortex, and cortex in the lateral sulcus. Contralaterally, labeled neurons were mostly in area 1. The results implicate portions of areas 3b, 3a, and 1 in the processing of tactile information from the teeth and tongue, and possibly taste information from the tongue.

Animals↗

Organization of primary afferent projections to the gracile nucleus of the dorsal column system of primates.

In order to reveal the somatotopic organization of the gracile nucleus of the dorsal column-trigeminal complex, neuroanatomical tracers were injected subcutaneously into various parts of the hindlimb and tail of prosimian galagos, New World monkeys, and Old World monkeys. In most cases, tracers were injected bilaterally, and into more than one body part. In six cases, two different, distinguishable tracers were injected into the same hindlimb. Brainstem and spinal cord sections were processed for tracers transported by cutaneous afferents to terminations in the gracile nuclei. Foci of terminations were related to the cell-cluster architecture of the gracile nuclei in sections processed for cytochrome oxidase or stained for cell bodies (Nissl stain). In all taxa, terminations labeled by the injections were distributed in a patchy fashion along the rostrocaudal length of the ipsilateral gracile nucleus. Terminations were largely but not completely focused within the cytochrome oxidase dense cell clusters. Across taxa, afferents from the tail, foot, lower leg, and upper leg terminated in a mediolateral sequence within the gracile nucleus. Afferents from the glabrous skin of toes 1-5 terminated in a ventromedial to dorsolateral sequence in owl, squirrel, and macaque monkeys, but an altered arrangement was seen in the galagos, with a ventrolateral location for toe 1. The use of two tracers in squirrel monkeys indicated that terminations from adjacent toes formed adjacent and largely segregated patches. Terminations of afferents from the plantar pad (sole) of the foot tended to surround those from the glabrous toes.

Afferent Pathways↗

Unequal representation of cardinal vs. oblique orientations in the middle temporal visual area.

A possible neurobiological basis for the "oblique effect" is linked to the finding that more neural machinery is devoted to processing cardinal vs. oblique orientations in primary visual cortex (V1). We used optical imaging to determine whether more territory is devoted to processing horizontal and vertical orientations than oblique orientations in owl monkey middle temporal visual area (MT), a visual area highly sensitive to moving stimuli. We found that more of MT was devoted to representing cardinal than oblique orientations, and that the anisotropy was more prominent in parts of MT representing central vision (< or =10 degrees). Neural responses to orientations of 0 degrees and 90 degrees were also greater than those to 45 degrees and 135 degrees . In comparison, an overrepresentation of cardinal orientations in the representation of central vision in owl monkey V1 was relatively small and inconsistent. Our data could explain the greater sensitivity to motion discrimination when stimuli are moved along cardinal meridians and suggest that the neural machinery necessary to explain the motion oblique effect either originates in MT or is enhanced at this level.

Animals↗

Organization of frontoparietal cortex in the tree shrew (Tupaia belangeri). I. Architecture, microelectrode maps, and corticospinal connections.

Despite extensive investigation of the motor cortex of primates, little is known about the organization of motor cortex in tree shrews, one of their closest living relatives. We investigated the organization of frontoparietal cortex in Belanger's tree shrews (Tupaia belangeri) by using intracortical microstimulation (ICMS), corticospinal tracing, and detailed histological analysis. The results provide evidence for the subdivision of tree shrew frontoparietal cortex into seven distinct areas (five are newly identified), including two motor fields (M1 and M2) and five somatosensory fields (3a, 3b, S2, PV, and SC). The types of movements evoked in M1 and M2 were similar, but M2 required higher currents to elicit movements and had few connections to the cervical spinal cord and distinctive cyto- and immunoarchitecture. The borders between M1 and the anterior somatosensory regions (3a and 3b) were identified primarily from histological analysis, because thresholds were similar between these regions, and differences in corticospinal neuron distribution were subtle. The caudal (SC) and lateral (S2 and PV) somatosensory fields were identified based on differences in architecture and distribution of corticospinal neurons. Myelin-dense modules were identified in lateral cortex, in the expected location of the oral, forelimb, and hindlimb representations of S2, and possibly PV. Evidence for a complex primate-like array of motor fields is lacking in tree shrews, but their motor cortex shares a number of basic features with that of primates, which are not found in more distantly related species, such as rats.

Animals↗

Ipsilateral cortical connections of dorsal and ventral premotor areas in New World owl monkeys.

In order to compare connections of premotor cortical areas of New World monkeys with those of Old World macaque monkeys and prosimian galagos, we placed injections of fluorescent tracers and wheat germ agglutinin-horseradish peroxidase (WGA-HRP) in dorsal (PMD) and ventral (PMV) premotor areas of owl monkeys. Motor areas and injection sites were defined by patterns of movements electrically evoked from the cortex with microelectrodes. Labeled neurons and axon terminals were located in brain sections cut either in the coronal plane or parallel to the surface of flattened cortex, and they related to architectonically and electrophysiologically defined cortical areas. Both the PMV and PMD had connections with the primary motor cortex (M1), the supplementary motor area (SMA), cingulate motor areas, somatosensory areas S2 and PV, and the posterior parietal cortex. Only the PMV had connections with somatosensory areas 3a, 1, 2, PR, and PV. The PMD received inputs from more caudal portions of the cortex of the lateral sulcus and more medial portions of the posterior parietal cortex than the PMV. The PMD and PMV were only weakly interconnected. New World owl monkeys, Old World macaque monkeys, and galagos share a number of PMV and PMD connections, suggesting preservation of a common sensorimotor network from early primates. Comparisons of PMD and PMV connectivity with the cortex of the lateral sulcus and posterior parietal cortex of owl monkeys, galagos, and macaques help identify areas that could be homologous.

Animals↗

Cortical network for representing the teeth and tongue in primates.

Sensory information from the tongue and teeth is used to evaluate and distinguish food and nonfood items in the mouth, reject some and masticate and swallow others. While it is known that primates have a complex array of 10 or more somatosensory areas that contribute to the analysis of sensory information from the hand, less is known about what cortical areas are involved in processing information from receptors of the tongue and teeth. The tongue contains taste receptors, as well as mechanoreceptors. Afferents from taste receptors and mechanoreceptors of the tongue access different ascending systems in the brainstem. However, it is uncertain how these two sources of information are processed in cortex. Here the parts of somatosensory areas 3b, 3a, and presumptive 1 that represent the mechanoreceptors of the teeth and tongue are identified, and evidence is presented that the representations of the tongue also get information from the taste nucleus of the thalamus, VPMpc. As areas 3b, 3a, and 1 project to other areas of somatosensory cortex, and those areas to additional areas, some or all of the currently defined somatosensory areas of cortex may be involved in processing gustatory, as well as tactile, information from the tongue and thus have a role in the biologically important function of evaluating food in the mouth.

Animals↗

Specializations of the granular prefrontal cortex of primates: implications for cognitive processing.

The biological underpinnings of human intelligence remain enigmatic. There remains the greatest confusion and controversy regarding mechanisms that enable humans to conceptualize, plan, and prioritize, and why they are set apart from other animals in their cognitive abilities. Here we demonstrate that the basic neuronal building block of the cerebral cortex, the pyramidal cell, is characterized by marked differences in structure among primate species. Moreover, comparison of the complexity of neuron structure with the size of the cortical area/region in which the cells are located revealed that trends in the granular prefrontal cortex (gPFC) were dramatically different to those in visual cortex. More specifically, pyramidal cells in the gPFC of humans had a disproportionately high number of spines. As neuron structure determines both its biophysical properties and connectivity, differences in the complexity in dendritic structure observed here endow neurons with different computational abilities. Furthermore, cortical circuits composed of neurons with distinguishable morphologies will likely be characterized by different functional capabilities. We propose that 1. circuitry in V1, V2, and gPFC within any given species differs in its functional capabilities and 2. there are dramatic differences in the functional capabilities of gPFC circuitry in different species, which are central to the different cognitive styles of primates. In particular, the highly branched, spinous neurons in the human gPFC may be a key component of human intelligence.

Animals↗

Neuroscience: rewiring the adult brain.

Any analysis of plastic reorganization at a neuronal locus needs a veridical measure of changes in the functional output--that is, spiking responses of the neurons in question. In a study of the effect of retinal lesions on adult primary visual cortex (V1), Smirnakis et al. propose that there is no cortical reorganization. Their results are based, however, on BOLD (blood-oxygen-level-dependent) fMRI (functional magnetic resonance imaging), which provides an unreliable gauge of spiking activity. We therefore question their criterion for lack of plasticity, particularly in the light of the large body of earlier work that demonstrates cortical plasticity.

Action Potentials↗

Ipsilateral cortical connections of motor, premotor, frontal eye, and posterior parietal fields in a prosimian primate, Otolemur garnetti.

The ipsilateral connections of motor areas of galagos were determined by injecting tracers into primary motor cortex (M1), dorsal premotor area (PMD), ventral premotor area (PMV), supplementary motor area (SMA), and frontal eye field (FEF). Other injections were placed in frontal cortex and in posterior parietal cortex to define the connections of motor areas further. Intracortical microstimulation was used to identify injection sites and map motor areas in the same cases. The major connections of M1 were with premotor cortex, SMA, cingulate motor cortex, somatosensory areas 3a and 1, and the rostral half of posterior parietal cortex. Less dense connections were with the second (S2) and parietal ventral (PV) somatosensory areas. Injections in PMD labeled neurons across a mediolateral belt of posterior parietal cortex extending from the medial wall to lateral to the intraparietal sulcus. Other inputs came from SMA, M1, PMV, and adjoining frontal cortex. PMV injections labeled neurons across a large zone of posterior parietal cortex, overlapping the region projecting to PMD but centered more laterally. Other connections were with M1, PMD, and frontal cortex and sparsely with somatosensory areas 3a, 1-2, S2, and PV. SMA connections were with medial posterior parietal cortex, cingulate motor cortex, PMD, and PMV. An FEF injection labeled neurons in the intraparietal sulcus. Injections in posterior parietal cortex revealed that the rostral half receives somatosensory inputs, whereas the caudal half receives visual inputs. Thus, posterior parietal cortex links visual and somatosensory areas with motor fields of frontal cortex.

Animals↗

The future of mapping sensory cortex in primates: three of many remaining issues.

After 100 years of progress in understanding the organization of cerebral cortex, three issues have persisted over the last 35 years, which are revisited in this paper. First, is V3 an established or questionable area of visual cortex? Second, does taste cortex include part of area 3b (S1 proper) and other somatosensory areas? Third, is primary auditory cortex, A1, of primates the homologue of A1 in cats? The existence of such questions about even the early stages of cortical processing reflects the difficulties in mapping cerebral cortex, and reminds us that the era of basic discovery is far from over.

Animals↗

Regional specialization in pyramidal cell structure in the visual cortex of the galago: an intracellular injection study of striate and extrastriate areas with comparative notes on new world and old world monkeys.

Recent studies have revealed marked differences in the basal dendritic structure of layer III pyramidal cells in the cerebral cortex of adult simian primates. In particular, there is a consistent trend for pyramidal cells of increasing complexity with anterior progression through occipitotemporal cortical visual areas. These differences in pyramidal cell structure, and their systematic nature, are believed to be important for specialized aspects of visual processing within, and between, cortical areas. However, it remains unknown whether this regional specialization in the pyramidal cell phenotype is unique to simians, is unique to primates in general or is widespread amongst mammalian species. In the present study we investigated pyramidal cell structure in the prosimian galago (Otolemur garnetti). We found, as in simians, that the basal dendritic arbors of pyramidal cells differed between cortical areas. More specifically, pyramidal cells became progressively more spinous through the primary (V1), second (V2), dorsolateral (DL) and inferotemporal (IT) visual areas. Moreover, pyramidal neurons in V1 of the galago are remarkably similar to those in other primate species, in spite of large differences in the sizes of this area. In contrast, pyramidal cells in inferotemporal cortex are quite variable among primate species. These data suggest that regional specialization in pyramidal cell phenotype was a likely feature of cortex in a common ancestor of simian and prosimian primates, but the degree of specialization varies between species.

Animals↗

Optical imaging of visually evoked responses in the middle temporal area after deactivation of primary visual cortex in adult primates.

The middle temporal area (MT) is a visual area in primates with direct and indirect inputs from the primary visual cortex (V1), a role in visual motion perception, and a suggested role in "blindsight." When V1 is deactivated, some studies report continued activation of MT neurons, which has been attributed to an indirect pathway to MT from the superior colliculus. Here we used muscimol to deactivate V1 while optically imaging visually evoked activity in MT in two primates, owl monkeys and galagos, where MT is exposed on the brain surface. The partial loss of V1 inputs abolished all or nearly all evoked activity in the retinotopically matched part of MT. Low levels of activation that persisted in portions of MT that were unstimulated or retinotopically congruent with the blocked portion of V1 appeared to reflect the spread of activity from stimulated to unstimulated parts of MT. Thus, a significant pathway based on the superior colliculus was not demonstrated.

Aging↗

Microstimulation reveals specialized subregions for different complex movements in posterior parietal cortex of prosimian galagos.

Posterior parietal cortex of prosimian galagos consists of a caudal half characterized by connections with visual cortex and a rostral half connected with motor, premotor, and visuomotor areas of frontal cortex. When 500-ms trains of electrical pulses were used to stimulate microelectrode sites throughout posterior parietal cortex, movements were elicited only from the rostral half. The movement zone reflected an overall pattern of somatotopy, from eye and face movements most ventrally to hindlimb movements most dorsally. In addition, subregions or zones of this movement cortex seemed to be devoted to components of different, ethologically significant behaviors. Thus, microstimulation within separate zones of cortex elicited reaching, hand-to-mouth, defensive, or aggressive movements. The finding of similar classes of elicited movement patterns from frontal and more recently intraparietal cortex of macaques suggests that multiareal circuits for biologically significant behaviors are components of all primate brains and that these circuits can be activated by long trains of current pulses at rostral locations in posterior parietal cortex.

Animals↗

Areal specialization of pyramidal cell structure in the visual cortex of the tree shrew: a new twist revealed in the evolution of cortical circuitry.

Cortical pyramidal cells, while having a characteristic morphology, show marked phenotypic variation in primates. Differences have been reported in their size, branching structure and spine density between cortical areas. In particular, there is a systematic increase in the complexity of the structure of pyramidal cells with anterior progression through occipito-temporal cortical visual areas. These differences reflect area-specific specializations in cortical circuitry, which are believed to be important for visual processing. However, it remains unknown as to whether these regional specializations in pyramidal cell structure are restricted to primates. Here we investigated pyramidal cell structure in the visual cortex of the tree shrew, including the primary (V1), second (V2) and temporal dorsal (TD) areas. As in primates, there was a trend for more complex branching structure with anterior progression through visual areas in the tree shrew. However, contrary to the trend reported in primates, cells in the tree shrew tended to become smaller with anterior progression through V1, V2 and TD. In addition, pyramidal cells in V1 of the tree shrew are more than twice as spinous as those in primates. These data suggest that variables that shape the structure of adult cortical pyramidal cells differ among species.

Animals↗

Pyramidal neurons of granular prefrontal cortex of the galago: complexity in evolution of the psychic cell in primates.

Typically, cognitive abilities of humans have been attributed to their greatly expanded cortical mantle, granular prefrontal cortex (gPFC) in particular. Recently we have demonstrated systematic differences in microstructure of gPFC in different species. Specifically, pyramidal cells in adult human gPFC are considerably more spinous than those in the gPFC of the macaque monkey, which are more spinous than those in the gPFC of marmoset and owl monkeys. As most cortical dendritic spines receive at least one excitatory input, pyramidal cells in these different species putatively receive different numbers of inputs. These differences in the gPFC pyramidal cell phenotype may be of fundamental importance in determining the functional characteristics of prefrontal circuitry and hence the cognitive styles of the different species. However, it remains unknown as to why the gPFC pyramidal cell phenotype differs between species. Differences could be attributed to, among other things, brain size, relative size of gPFC, or the lineage to which the species belong. Here we investigated pyramidal cells in the dorsolateral gPFC of the prosimian galago to extend the basis for comparison. We found these cells to be less spinous than those in human, macaque, and marmoset.

Animals↗

Distribution across cortical areas of neurons projecting to the superior colliculus in new world monkeys.

Surprisingly little is known about the proportions of projections of different areas and regions of neocortex to the superior colliculus in primates. To obtain an overview of such projection patterns, we placed a total of 10 injections of retrograde tracers in the superior colliculus of three New World monkeys (Callithrix, Callicebus, and Aotus). Because cortex was flattened and cut parallel to the surface, labeled corticotectal neurons could be accurately located relative to architectonic boundaries and surface features. While there was variability across cases and injection sites, the summed results clearly support several conclusions. One, three well-defined visual areas, V1 (18%), V2 (14%), and MT (11%), contributed nearly half of the total of labeled cells. Two, several other visual areas (V3, DL, DM, and FST) that are early in the processing hierarchy provided another fifth of the total. Three, inferior temporal visual areas of the ventral stream provided only minor projections. Four, visuomotor fields (FEF, FV, cortex in the region of SEF, and posterior parietal cortex) contained less than 10% of the labeled neurons. Five, few labeled neurons were in auditory or somatosensory areas. The results indicate that cortical inputs to the superior colliculus originate predominantly from early visual areas rather than from multimodal or visuomotor areas.

Afferent Pathways↗