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C R Olson

Publications and source records attributed to C R Olson.

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Topographic organization of cortical and subcortical projections to posterior cingulate cortex in the cat: evidence for somatic, ocular, and complex subregions.

The posterior cingulate area (CGp) of the cat consists of cortex on the exposed cingulate gyrus and in the adjacent ventral bank of the splenial sulcus. We have placed deposits of distinguishable fluorescent tracers at multiple restricted sites in CGp and have analyzed the distribution throughout the forebrain of neurons labeled by retrograde transport. Cortical projections to CGp arise (in approximately descending order of strength) from anterior cingulate cortex; prefrontal cortex and premotor areas including the frontal eye fields; visual areas including especially areas 7 and 20b; parahippocampal areas; insular cortex; somesthetic areas; and auditory areas. Corticocortical pathways are organized topographically with respect to the posterior-anterior axis in CGp. Projections from prefrontal cortex and other areas with complex (as opposed to sensory, motor, or limbic) functions are concentrated posteriorly; projections from visual and oculomotor areas are concentrated at an intermediate level; and projections from areas with somesthetic and somatomotor functions are concentrated anteriorly. Thalamic projections to CGp arise from the anterior nuclei (AD, AV, and AM), from restricted portions of the ventral complex (VAd, VAm, and VMP), from discrete sectors of the lateral complex (LD, LPs, and LPm), from the rostral crescent of intralaminar nuclei (CM, PC, and CL), and from the reuniens nucleus. Projections from AM, VAd, LD, and LPs are spatially ordered in the sense that more ventral thalamic neurons project to more anterior cortical sites. Projections from AV and AD are stronger at more posterior cortical sites but do not show other signs of topographic ordering. Projections from LPm, CM, PC, CL, and RE are diffuse. We conclude (1) that cortical afferents of CGp derive predominantly from neocortical areas including those with well established sensory and motor functions; (2) that limbic projections to CGp originate primarily in structures, including the hippocampus, which are associated with memory, as opposed to structures, including the amygdala, which are associated with emotional and instinctual behavior; and (3) that CGp contains subregions in which complex, ocular, or somatic afferents predominate.

Afferent Pathways

Cortical areas in the medial frontal lobe of the cat delineated by quantitative analysis of thalamic afferents.

The aim of these experiments was to establish the number and location of connectionally distinct areas in the medial frontal lobe of the cat. Thirty deposits of distinguishable retrograde tracers were placed at restricted sites spanning the medial frontal lobe in 16 cats. Following each deposit, the number of retrogradely labeled neurons in each of 17 thalamic nuclei was determined. Variations of the thalamic labeling pattern dependent on the location of the cortical tracer deposit were then analyzed by a quantitative procedure. The results indicate that the medial frontal lobe contains three fundamental divisions: the anterior cingulate area, medial area 6, and the medial prefrontal district. The anterior cingulate area derives its strongest thalamic input from the anteriomedial nucleus. Medial area 6 is the target of afferents originating in a dorsolateral sector of the mediodorsal nucleus and in the ventroanterior nucleus. Medial prefrontal cortex is heavily innervated by pathways originating in the core of the mediodorsal nucleus and in the principal ventromedial nucleus. Within each major district, thalamic connectional patterns exhibit graded regional variation, with the result that, whereas the connections of the district are not uniform, it is difficult to define further discrete subdivisions. We discuss these results in relation to previously proposed schemes for paracellation of the cat's medial frontal lobe and conclude that the infralimbic and prelimbic areas (areas 25 and 32) of previous systems are best understood not as discrete areas but as ventral and intermediate sectors of a continuous medial prefrontal domain.

Afferent Pathways

Organization of cortical and subcortical projections to anterior cingulate cortex in the cat.

The aim of the experiments reported here was to identify cortical and subcortical forebrain structures from which anterior cingulate cortex (CGa) receives input in the cat. Deposits of retrograde tracers were placed at nine sites spanning the anterior cingulate area and patterns of retrograde transport were analyzed. Thalamic projections to CGa, in descending order of strength, originate in the anteromedial nucleus, lateroposterior nucleus, ventroanterior nucleus, rostral intralaminar complex, reuniens nucleus, mediodorsal nucleus, and laterodorsal nucleus. Minor and inconsistent ascending pathways arise in the paraventricular, parataenial, parafascicular, and subparafascicular thalamic nuclei. The basolateral nucleus of the amygdala, the hypothalamus, the nucleus of the diagonal band, and the claustrum are additional sources of ascending input. Cortical projections to CGa, in descending order of strength, derive from posterior cingulate cortex, prefrontal cortex, motor cortex (areas 4 and 6), parahippocampal cortex (entorhinal, perirhinal, postsubicular, parasubicular, and subicular areas), insular cortex, somesthetic cortex (areas 5 and SIV), and visual cortex (areas 7p, 20b, AMLS, PS and EPp). In general, the limbic, sensory, and motor afferents of CGa are weak. The dominant sources of input to CGa are other cortical areas with high-order functions. This finding calls into question the traditional characterization of cingulate cortex as a bridge between neocortical association areas and the limbic system.

Afferent Pathways

Organization of cortical and subcortical projections to medial prefrontal cortex in the cat.

We have analyzed the cortical and subcortical afferent connections of the medial prefrontal cortex (MPF) in the cat with the specific aim of characterizing subregional variations of afferent connectivity. Thirteen tracer deposits were placed at restricted loci within a cortical district extending from the proreal to the subgenual gyrus. The distribution throughout the forebrain of retrogradely labeled neurons was then analyzed. Within the thalamus, retrogradely labeled neurons were most numerous in the mediodorsal nucleus and in the ventral complex. The projection from each region exhibited continuous topography such that more medial thalamic neurons were labeled by tracer from more ventral and posterior cortical deposits. Marked retrograde labeling without any sign of topographic order occurred in a narrow medioventral sector of the lateroposterior nucleus. Several additional thalamic nuclei contained small numbers of labeled neurons. In a subset of nuclei closely affiliated with the limbic system (the parataenial, paraventricular, reuniens, and basal ventromedial nuclei), retrograde labeling occurred exclusively after deposits at extremely ventral and posterior cortical sites. Within the amygdala, retrogradely labeled neurons occupied the anterior basomedial nucleus, the posterior basolateral nucleus, and a narrow strip of the lateral nucleus immediately adjoining the basolateral nucleus. The number of labeled neurons was greater after more ventral deposits. Very ventral deposits resulted in extensive labeling of the cortical amygdala. Within the cerebral cortex, the distribution of labeled neurons depended on the location of the tracer deposit. Comparatively dorsal deposits produced prominent retrograde transport to the anterior and posterior cingulate areas, to the agranular insula, and to lateral prefrontal cortex. Comparatively ventral deposits gave rise to prominent labeling of the hippocampal subiculum, various parahippocampal areas, and prepiriform cortex. On the basis of afferent connections, it is possible to divide the cat's medial prefrontal cortex into an infralimbic component, MPFil, marked by strong afferents from prepiriform cortex and the cortical amygdala, and a dorsal component, MPFd, without afferents from these structures. Further, within MPFd, it is possible to define an axis, running from ventral and posterior to dorsal and anterior levels, along which limbic afferents gradually become weaker and projections from cortical association areas gradually become stronger.

Acetylcholinesterase

Visual and auditory association areas of the cat's posterior ectosylvian gyrus: thalamic afferents.

The feline posterior ectosylvian gyrus contains a broad band of association cortex that is bounded anteriorly by tonotopic auditory areas and posteriorly by retinotopic visual areas. To characterize the possible functions of this cortex and to throw light on its pattern of internal divisions, we have carried out an analysis of its thalamic afferents. Deposits of differentiable retrograde tracers were placed at 17 cortical sites in nine cats. The deposit sites spanned the crown of the posterior ectosylvian gyrus and adjacent cortex in the suprasylvian sulcus. We compiled counts of retrogradely labeled neurons in 12 thalamic nuclei delineated by use of Nissl and acetylcholinesterase stains. We then employed a statistical clustering algorithm to identify groups of injections that gave rise to similar patterns of thalamic labeling. The results suggest that the posterior ectosylvian gyrus contains 3 fundamentally different cortical districts that have the form of parallel vertical bands. Very anterior cortex, overlapping previously identified tonotopic auditory areas (AI, P and VP) receives a dense projection from the laminated division of the medial geniculate body (MGl). An intermediate strip, to which we refer as the auditory belt, is innervated by axons from nontonotopic divisions of the medial geniculate body (MGds, MGvl, MGm, and MGd), from the lateral division of the posterior group (Pol), and from the posterior suprageniculate nucleus (SGp). A posterior strip, to which we refer as EPp, receives strong projections from the LM-SG complex (LM-SGa and LMp), and lighter projections from the intralaminar and lateroposterior (LPm and LPl) nuclei. On grounds of thalamic connectivity, EPp is not obviously distinguishable from adjacent retinotopic visual areas (PLLS, DLS, and VLS), and may be regarded as forming, together with these areas, a connectionally homogeneous visual belt.

Animals

Visual and auditory association areas of the cat's posterior ectosylvian gyrus: cortical afferents.

In a preceding report, we described patterns of thalamic retrograde labeling following 17 tracer deposits on the cat's posterior ectosylvian gyrus and concluded, on the basis of patterns of thalamic connectivity, that the posterior ectosylvian gyrus is composed of three major divisions: a tonotopic auditory zone located anteriorly, a belt of auditory association cortex occupying the gyral crown, and a visual belt located posteriorly. We describe here patterns of transcortical retrograde labeling obtained from tracer deposits in the three zones so defined. Our results indicate that the tonotopic auditory strip is innervated primarily by axons from low-order auditory areas (AAF, AI, P, VP, and V), that the auditory belt receives its strongest input from nontonotopic auditory fields (AII, temporal cortex, and other parts of the auditory belt), and that projections to the visual belt derive primarily from extrastriate visual areas (ALLS, PLLS, DLS, 19, 20, and 21) and from association areas affiliated with the visual system (insular cortex, posterior cingulate gyrus, area 7p, and frontal cortex). We discuss the results in relation to previous systems for parcellating the posterior ectosylvian gyrus of the cat and consider the possibility that divisions of the feline posterior ectosylvian gyrus correspond directly to areas making up the superior temporal gyrus in primates.

Animals

Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study.

We have examined the origin and topography of cortical projections to area PO, an extrastriate visual area located in the parieto-occipital sulcus of the macaque. Distinguishable retrograde fluorescent tracers were injected into area PO at separate retinotopic loci identified by single-neuron recording. The results indicate that area PO receives retinotopically organized inputs from visual areas V1, V2, V3, V4, and MT. In each of these areas the projection to PO arises from the representation of the periphery of the visual field. This finding is consistent with neurophysiological data indicating that the representation of the periphery is emphasized in PO. Additional projections arise from area MST, the frontal eye fields, and several divisions of parietal cortex, including four zones within the intraparietal sulcus and a region on the medial dorsal surface of the hemisphere (MDP). On the basis of the laminar distribution of labeled cells we conclude that area PO receives an ascending input from V1, V2, and V3 and receives descending or lateral inputs from all other areas. Thus, area PO is at approximately the same level in the hierarchy of visual areas as areas V4 and MT. Area PO is connected both directly and indirectly, via MT and MST, to parietal cortex. Within parietal cortex, area PO is linked to particular regions of the intraparietal sulcus including VIP and LIP and two newly recognized zones termed here MIP and PIP. The wealth of connections with parietal cortex suggests that area PO provides a relatively direct route over which information concerning the visual field periphery can be transmitted from striate and prestriate cortex to parietal cortex. In contrast, area PO has few links with areas projecting to inferior temporal cortex. The pattern of connections revealed in this study is consistent with the view that area PO is primarily involved in visuospatial functioning.

Animals

Organization of cortical and subcortical projections to area 6m of the cat.

By analyzing regional variations of afferent connectivity, we have identified a medial subdivision of feline area 6 (area 6m) which differs from all surrounding sectors of the frontal lobe in its pattern of inputs. Area 6m is located in the ventral bank of the cruciate sulcus and on the adjacent medial face of the frontal lobe and is partially coextensive with the medial frontal eye field as identified previously in electrophysiological experiments. Area 6m is innervated by axons from visual, association, and oculomotor areas and does not receive projections from somesthetic or somatomotor areas. Cortical sources of input to area 6m include several retinotopically organized extrastriate visual areas (AMLS, ALLS, and PLLS), association areas with strong links to the visual system (area 7, granular insula, posterior ectosylvian gyrus, and cingulate gyrus), and a lateral division of area 6 (area 61) with oculomotor functions. Thalamic afferents of area 6m derive from the paralamellar ventral anterior nucleus, from a dorsolateral division of the mediodorsal nucleus, and from the rostral intralaminar nuclei. The claustrum and the basolateral nucleus of the amygdala project to area 6m. Projections from area 7, the posterior cingulate area, the ventral anterior nucleus, and the mediodorsal nucleus are spatially ordered in a pattern such that parts of area 6 close to the fundus of the cruciate sulcus receive input from neurons positioned anteriorly in the cortical areas, dorsolaterally in the ventral anterior nucleus, and ventrolaterally in the mediodorsal nucleus. Our results indicate that area 6m probably is involved in the voluntary control of gaze and attention rather than in skeletomotor functions.

Afferent Pathways

Cortical and subcortical afferent connections of a posterior division of feline area 7 (area 7p).

Area 7 of the cat, as identified cytoarchitecturally, includes cortex both on the middle suprasylvian gyrus and on the anterior lateral gyrus. The aim of the experiments reported here was to determine whether within this zone there are subdivisions with qualitatively different patterns of afferent connectivity. Deposits of distinguishable retrograde tracers were placed at 29 sites in and around area 7 of 15 cats; cortical and subcortical telencephalic structures were then scanned for retrograde labeling. Our results indicate that cortex on the anterior lateral gyrus, although often included in area 7, is indistinguishable on connectional grounds from adjacent somesthetic cortex (area 5b). Cortex with strong links to visual, oculomotor, and association areas is confined to the middle suprasylvian gyrus and the adjacent lateral bank of the lateral sulcus. We refer to this discrete, connectionally defined zone as posterior area 7 (area 7p). Area 7p receives input from visual areas 19, 20a, 20b, 21a, 21b, AMLS, ALLS, and PLLS; from frontal oculomotor cortex (areas 6m and 6l); and from cortical association areas (posterior cingulate cortex, the granular insula, the posterior ectosylvian gyrus, and posterior area 35). Thalamic projections to area 7p arise from three specific nuclei (pulvinar; nucleus lateralis intermedius, pars caudalis; nucleus ventralis anterior) and from the intralaminar complex (nuclei centralis lateralis, paracentralis and centralis medialis). Neurons in a division of the claustrum immediately beneath the somatosensory and visual zones project to area 7p. Within area 7p, anterior-posterior regional differentiation is present, as indicated by the spatial ordering of projections from cingulate and frontal cortex, the thalamus, and the claustrum. Area 7p, as delineated by connectional analysis in this study, resembles cortex of the primate inferior parietal lobule both in its location relative to other cortical districts and in its pattern of neural connectivity.

Animals

Eye alignment in kittens.

1. The alignment of the pupillary axes and of the visual axes has been measured in 23 normally reared cats ranging in age from 14 days to adulthood. 2. In agreement with a previous report, we find that pupillary divergence, as measured from photographs, tends to decrease during the first 2 mo of life. 3. The angle between the visual axes of cats of various ages was determined during paralysis by plotting the receptive fields of neurons in cortical area 17, and extrapolation to the angle of alignment of the freely moving animal was accomplished by comparing pupillary photographs taken before and after immobilization. Results obtained by this method reveal that in cats of all ages the visual axes are convergent, and that the average angle of convergence is approximately the same at all ages. 4. We conclude that young kittens may be capable of coordinated binocular vision. Further study will be required to determine whether animals as young as 2 wk are able to align their eyes accurately so as to bring the two retinal images of object space into register. 5. Pupillary divergence decreases during development as a result of changes in the geometry of the eye characterized by a reduction of the angle between the pupillary axis and the visual axis in each eye. This angle changes from around 25 degrees at 14 days to around 16 degrees in adulthood. 6. The role of visual experience in the maintenance of normal eye alignment was investigated by rearing five cats in darkness until the age of 4-7 mo. In three animals, visual axis alignment was within the normal range. The two remaining cats were slightly exotropic. 7. A change occurs during development in the apparent cyclotorsional alignment of the eyes, as determined by measuring the intorsional angle formed by the two slit pupils. This angle increases during the 1st and 2nd mo, assuming a mean value of 14 degrees. In dark-reared cats the increase continues through the 3rd mo, culminating in an abnormally large angle of pupillary intorsion (mean of 24 degrees). The possibility that these changes reflect true shifts in cyclotorsional alignment of the eyes is discussed.

Animals

Progressive changes in kitten striate cortex during monocular vision.

Following initial rearing in either total darkness or normal illumination, kittens at different ages were subjected to right-eye closure and various periods of vision through the left eye. After the period of monocular vision, single units in striate cortex were tested for visual responsiveness through each eye. A severe reduction in the proportion of units responsive to the deprived eye occurred over the first few days of monocular vision. Functional abnormalities were variably present after 1 day, marked after 2.5 and 3.5 days, and complete after 10 days. Monocular vision produced very much the same effect on ocular dominance of striate units, provided age and duration of suture were identical, regardless of whether kittens had received prior dark- or light-rearing.

Animals

Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions.

The cingulate gyrus is a major part of the "anatomical limbic system" and, according to classic accounts, is involved in emotion. This view is oversimplified in light of recent clinical and experimental findings that cingulate cortex participates not only in emotion but also in sensory, motor, and cognitive processes. Anterior cingulate cortex, consisting of areas 25 and 24, has been implicated in visceromotor, skeletomotor, and endocrine outflow. These processes include responses to painful stimuli, maternal behavior, vocalization, and attention to action. Since all of these activities have an affective component, it is likely that connections with the amygdala are critical for them. In contrast, posterior cingulate cortex, consisting of areas 29, 30, 23, and 31, contains neurons that monitor eye movements and respond to sensory stimuli. Ablation studies suggest that this region is involved in spatial orientation and memory. It is likely that connections between posterior cingulate and parahippocampal cortices contribute to these processes. We conclude that there is a fundamental dichotomy between the functions of anterior and posterior cingulate cortices. The anterior cortex subserves primarily executive functions related to the emotional control of visceral, skeletal, and endocrine outflow. The posterior cortex subserves evaluative functions such as monitoring sensory events and the organism's own behavior in the service of spatial orientation and memory.

Amygdala

Posterior cingulate cortex: sensory and oculomotor properties of single neurons in behaving cat.

The posterior cingulate cortex of the cat is strongly linked to cortical areas with sensory and oculomotor functions. We have now recorded from feline posterior cingulate neurons in order to determine whether they are active in conjunction with sensory events and eye movements. The results described here are based on monitoring the electrical activity of 195 single neurons in the posterior cingulate cortex of three cats equipped with surgically implanted scleral search coils and trained to fixate visual targets. Posterior cingulate neurons carry tonic orbital position signals and are phasically active in conjunction with saccadic eye movements. Activity related to eye movements and gaze is attenuated but not abolished by the elimination of visual feedback. Posterior cingulate neurons also are responsive to visual, auditory, and somatosensory stimulation. Systematic testing with visual stimuli revealed that responses are sharply reduced due to refractoriness at rates of stimulation greater than a few per second. These results conform to the theory that posterior cingulate cortex is involved in processes underlying visuospatial cognition.

Acoustic Stimulation