L.A. Benevento

Auditory-visual interaction in single cells in the cortex of the superior temporal sulcus and the orbital frontal cortex of the macaque monkey

Abstract Previous anatomical studies show that the cortex of the superior temporal sulcus and the orbital frontal cortex receive convergent corticocortical and thalamocortical projections which represent different sensory modalities. In the present experiments both intracellular and extracellular recordings were made in these cortical regions to determine if the individual cells receive polysensory information and if interactions between different medalities are a result of local convergence at the cortical cell. The results show that many neurons have visual receptive fields which are bilateral, include the fovea, and are sensitive to moving stimuli. Many of these neurons are also excited or inhibited by auditory stimuli. For both modalities a variety of ON or OFF excitatory and inhibitory effects was seen. The results further indicate that neurons in both regions show auditory-visual interactions and that at least some of these interactions are due to convergence at the cortical cell. For example, we found that auditory stimuli of a specific frequency had a powerful inhibitory effect on many of the neurons and that this inhibitory effect could negate the excitation caused by a visual stimulus. These types of interactions are related to the anatomical inputs and may be possible mechanism implicating each of these regions in attention and discrimination.

An autoradiographic study of the projections of the pretectum in the rhesus monkey (Macaca mulatta): evidence for sensorimotor links to the thalamus and oculomotor nuclei.

Autordiographic tracing methods were used to determine the differential projections of the pretectal nuclei, in the rhesus monkey, in relation to their inputs. The sublentiform (SL) and olivary (ON) nuclei receive projections from the visual cortex, superior colliculus (SC) and equal bilateral projection from the retina. The nucleus of the posterior commissure (NPC) and its subdivisions do not receive any of these inputs. The projections of the pretectum involve a number of structures within the thalamus and brain stem and there are differences in the projection targets of the pretectal region which receives direct visual input (i.e., SL and ON) and the region which does not (i.e., nucleus of the posterior commissure, NPC). For example, while all pretectal regions project within the pretectum and to the SC, accessory oculomotor nuclei, reticular formation, intralaminar nuclei and hypothalamus, it is only the retinorecipient zone which projects to rostral regions such as the visceral oculomotor nuclei, the lateral pulvinar, the border between the lateral pulvinar and medial pulvinar, the oral pulvinar as well as to the thalamic reticular nucleus, ventral lateral geniculate nucleus, zona incerta and other structures. It is concluded that the retina, SC and cortex which influence the visceral oculomotor nuclei can only do so by virtue of their projections to the pretectum, and that any consideration of accommodative and pupillary reflexes must view the pretectum as an obligatory link through which various structures can influence the intrinsic musculature of the eye. In contrast to the SC, the pretectum does not project to any of the visual relay nuclei of the thalamus, such as the inferior pulvinar, which project to the visual cortices. Instead, the pretectum projects directly to visuomotor, visceromotor and arousal systems.

A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey.

Both anterograde and retrograde transport tracing methods were used to study the organization of the projections of the dorsal lateral geniculate (DLG), the inferior pulvinar and subdivisions of the lateral pulvinar to primary visual cortex (striate cortex or area 17). The DLG projects only to striate cortex. These projections are retinotopically organized, and do not extend to any cortical layers above layer IVA. In contrast the inferior pulvinar (PI) and the immediately adjacent portion of the lateral pulvinar (PL alpha 48) project to both striate and prestriate cortex. The projections from these two thalamic areas to the striate cortex are also retinotopically organized and exist in parallel with those from the DLG. In contrast to the DLG, the projections from PI and PL alpha terminate above layer IVA in striate cortex, i.e. layers I, II and III. In prestriate cortex the layers of termination include layers IV, III and I. The pulvinar terminations in layers II and III of area 17 occur in segregated patches as do the geniculate terminations in layers IVC and IVA. On the other hand the pulvinar terminations in layer I which overlie those in layers II and III of area 17 appeared to be continuous. Control studies show that the remainder of the lateral pulvinar overlying PL alpha does not project to striate cortex. It is concluded that there are 3 visuotopically organized inputs from the lateral thalamus to primary visual cortex and that each of these inputs have different layers of termination. The inputs from PI and DLG can convey direct retinal inputs while those from PI and PL alpha can also be involved in intrinsic cortico-thalamocortical connection with prestriate cortex. It remains, then that it cannot be tacitly assumed that the ascending inputs which influence the response properties of the primary cortical neurons arise solely from the dorsal lateral geniculate nucleus. It is also argued that these inputs to the supragranular layers may be excitatory as those from the DLG to the IVth layer.

Extrageniculate thalamic projections to the primary visual cortex

Until recently, it was assumed that the dorsal lateral geniculate nucleus (DLG) alone was the sole source of thalamic input to the primary visual cortex of the cat. However, in other mammals, such as the macaque monkey 1-3,13,14, extrageniculate thalamic inputs to primary visual cortex (area 17) have been demonstrated. In the cat, part of the lateral posterior complex is now suspected to also provide extrageniculate thalamic input to primary visual cortex 6,15. Since the cat visual system has been heavily studied as a mammalian model, we were interested in discovering and characterizing the extrageniculate thalamocortical projections to area 17 which might exist in this species, and also in comparing the organization of these projections with the organization of analogous projections in other mammals. Horseradish peroxidase (HRP) and autoradiographic tracing techniques were used. Two to three injections of 0.15 tzl of 30 ~ HRP (Sigma VI) in sterile water were made bilaterally in each visual cortex of 4 animals. After 48 h the animals were perfused transcardially and 60 #m frozen sections were reacted for peroxidase by the benzidine dihydrochloride method 11. For the autoradiographic tracing studies the technique was the same as that previously used in this laboratory 3. Bilateral injections of 0.3-0.5/~1 of a sterile saline solution containing L-[2,3-aH]proline (10/~Ci/~l, spec. act. 39.7 Ci/mmol) and L-[4,5-SH]leucine (10 ~Ci/bd, spec. act. 5.0 Ci/mmol) were made, at a rate of 0.3 #l/h, in the thalamus of 6 cats which then survived for 3-7 days. The injection targets were those areas which had contained HRP-positive cells in the previous cases. Before presenting the results it is useful to define the anatomy of the pertinent thalamic regions. Connectional studies4A s have subdivided the lateral posterior complex into 3 parallel zones (Fig. 1). The most lateral zone or LPr, consists of the

The projection of occipital cortex to the dorsal lateral geniculate nucleus in the rhesus monkey (Macaca mulatta)

Abstract Large lesions were made in the occipital cortex of rhesus monkeys and the subsequent degeneration in the dorsal lateral geniculate nucleus was analyzed with the Fink-Heimer technique. Evidence was found for both anterograde and retrograde degeneration in the dorsal lateral geniculate nucleus. Moderately dense pericellular and terminal degeneration was found in all layers of the dorsal lateral geniculate nucleus. In addition, in all layers of the dorsal lateral geniculate nucleus, some cells undergoing retrograde degeneration exhibited a Fink-Heimer positive argyrophilia that was interpreted as being different from the argyrophilia associated with anterograde degeneration. It is concluded that the occipital cortex projects to the dorsal lateral geniculate nucleus in the rhesus monkey. These results are consistent with the reports for other primate and nonprimate species that show a direct projection from the occipital cortex to the dorsal lateral geniculate nucleus.

The projection of occipital cortex to orbital cortex in the rhesus monkey (Macaca mulatta)

Abstract Near total lesions of occipital cortex were made in rhesus monkeys and the subsequent anterograde degeneration was analyzed using the Fink-Heimer technique. In addition to degenerated terminal endings seen in parietal, temporal and frontal cortices, sparse to moderately dense pericellular and terminal degeneration was seen in posterior portions of ventral orbital cortex and the inferior prefrontal convexity (lateral orbital cortex). These results indicate that activity from the visual cortex may directly influence cells of the frontal orbital cortex.

Projections of lateral orbital cortex to sensory relay nuclei in the rhesus monkey.

In previous physiological studies 1,6,7,9 we have described some of the response characteristics of single units in the lateral orbital cortex of the rhesus monkey. Most of the units were found to be multimodal, responding to both visual and auditory stimuli. On the basis of its afferent connections the lateral orbital cortex is thought to be one of the major cortical areas receiving convergent multimodal sensory input. On the basis of these physiological and anatomical findings, we were interested in determining if the physiologically defined areas of lateral orbital cortex project to the subcortical nuclei of the ascending sensory systems that ultimately converge on the lateral orbital cortex. The cortical areas involved in the present study and previous physiological experiments included Walkers 27 area 12, area 6B/~ and portions of area 10 of the Vogts % and area fcd and postero-lateral area fd of Von Bonin and Bailey 26. Five young adult rhesus monkeys, Macaca mulatta, weighing 2.4-4.5 kg were used in the study. The animals were prepared for surgery and the brains were processed by the Fink-Heimer technique 1° as we have previously described 2,8. Three animals received cortical lesions in various sectors of lateral orbital cortex (Fig. 1). Two received control lesions in more dorsal sectors of prefrontal cortex. On the basis of the results of the control lesions it was concluded that lateral orbital lesions did not interrupt corticosubcortical fibers of passage from dorsal prefrontal areas. Survival times range from 7-14 days. The results in one animal from the first group (Rh 2387) which were typical of the results from the other two cases are illustrated here. The axons that degenerated as a result of the lateral orbital lesions were of fine caliber. Degenerating fiber tracts from the lesion site traversed the internal capsule and gave rise to pericellular degeneration in the rostral region of the thalamic reticular nucleus (Fig. 2, level I076). Other bundles of degenerating fibers from the internal capsule and inferior thalamic peduncle gave rise to pericellular and terminal degeneration in the following nuclei: anterodorsal and anteroventral nuclei (Fig. 2, level 1036), intralaminar nuclei including the paracentral, centrolateral, centromedian and para-

Classically conditioned limb reflexes reinforced by motor cortex stimulation

Abstract This study measures the latencies of, and the effect of the reduction of the interreinforcement time interval upon, conditional limb reflexes reinforced to an auditory conditional stimulus with movement evoking electrical stimulation of the motor-sensory cortex as the unconditional stimulus. Conditioned head movements were obtained in all, while limb movements developed in only 2, of 3 cats following 4.6 min reinforcement intervals. One-min reinforcement intervals did not abolish these limb responses which are here shown to have a latency significantly in excess of 1 sec. The conditional limb responses of this study are identified as a classical, as contrasted with the instrumental variant of other studies. The classical limb response is thought to develop if there is: (a) an absence of head movement induced extensor tonus; (b) a motor-sensory cortex stimulus adequate to evoke limb movement; and, (c) a period of conditional stimulus isolation ample to permit the observation of these long latency responses.