Receptive field changes after strokelike cortical ablation: a role for activation dynamics.

The reorganization of neural activity that takes place after stroke is of paramount importance in producing functional recovery. Experimental stroke models have suggested that this reorganization may have two phases, but physiology alone cannot fully resolve what causes each phase. Computer modeling suggests that these phases might involve an initial change in dynamics occurring immediately, followed by synaptic plasticity. We combined physiological recording from macaque middle temporal cortex (area MT) with a neural network computer model to examine this first phase of altered cortical function after a small, experimentally induced cortical lesion. Major receptive field (RF) changes seen in the first few days postlesion included both expansion and contraction of receptive fields. Although only expansion could be reproduced in an initial model, addition of inhibitory interneuron loss in a ring around the primary ablation, suggested by immunohistochemical examination, permitted contraction to be replicated as well. We therefore predict that this immunochemical observation reflects an immediate extension of the lesion rather than a late response. Additionally our model successfully predicted a correlation between increased firing rate and RF size. Our model suggests that activation dynamics alone, without anatomic remodeling, can cause the large receptive field changes that allow the rapid behavioral recovery seen after middle temporal lesions.

Recovery of function after lesions in the superior temporal sulcus in the monkey.

1. Ibotenic acid lesions in the monkey's middle temporal area (MT) and the medial superior temporal area (MST) in the superior temporal sulcus (STS) have previously been shown to produce a deficit in initiation of smooth-pursuit eye movements to moving visual targets. The deficits, however, recovery within a few days. In the present experiments we investigated the factors that influence that recovery. 2. We tested two aspects of the monkey's ability to use motion information to acquire moving targets. We used eye-position error as a measure of the monkey's ability to make accurate initial saccades to the moving target. We measured eye speed within the first 100 ms after the saccade to evaluate the monkey's initial smooth pursuit. 3. We determined that pursuit recovery was not dependent specifically on the use of neurotoxic lesions. Although the rate of recovery was slightly altered by replacing the usual neurotoxin (ibotenic acid) with another neurotoxin [alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)] or with an electrolytic lesion, pursuit recovery still occurred within a period of days to weeks. 4. There was a relationship between the size and location of the lesion and the recovery time. The time to recovery for eye-position error and initial eye speed increased with the fraction of MT removed. Whether the rate of recovery and size of lesions within regions on the anterior bank were related was unresolved. 5. We found that a large AMPA lesion within the STS that removed all of MT and nearly all of MST drastically altered the rate of recovery. Recovery was incomplete more than 7 mo after the lesion. Even with this lesion, however, the monkey's ability to use motion information for pursuit was not completely eliminated. 6. The large lesion also included parts of areas V1, V2, V3, and V4, but analysis of the visual fields associated with this lesion indicated that these areas probably did not have a substantial effect on recovery. 7. We tested whether visual motion experience of the monkey after a lesion was necessary for recovery by limiting the monkey's experience either by using a mask or by using 4-Hz stroboscopic illumination. In one monkey the eye-position error component of pursuit was prolonged to greater than 2 wk, but recovery of eye speed was not. Reduced motion experience had little effect on recovery in the other two monkeys. These results suggest that such visual motion experience is not necessary for the recovery of pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)

Somatosensory neurons projecting from the superior colliculus to the intralaminar thalamus in the rat.

Neurons of the rat superior colliculus projecting to the intralaminar thalamus were tested for their responses to somatosensory stimulation. They were identified by antidromic stimulation of the parafascicular nucleus and central lateral nucleus. To establish the existence of descending as well as ascending axon collaterals antidromic stimulation was applied to the upper cervical spinal cord in some cases. Somatosensory receptive fields were delineated and their laminar location in the superior colliculus was noted. Units were distributed throughout the intermediate and deep tectal layers, none were located in the superficial layers. Units with somatosensory receptive fields could be classified as low threshold, high threshold, wide dynamic range or complex. The majority of the peripherally responsive units (52%) were low threshold somatosensory units with contralateral receptive fields. All units were distributed throughout the intermediate and deep layers. Their distribution reflected the typical somatotopic organization of the superior colliculus. These results indicate that the intralaminar thalamus receives some sensory information by way of the tectum. In turn, the basal ganglia may gain direct access to this information by way of the thalamoneostriatal projection.

A grid system and a microsyringe for single cell recording.

The designs of two instruments are presented which have proven to be useful in single cell and chemical injection studies performed in awake monkeys. The first is a plastic grid that acts as a guide to produce parallel penetrations with either a microelectrode or microsyringe. The second is a syringe for injecting microliter quantities of a solution that also allows recording of neuronal activity.

Superior collicular projection to intralaminar thalamus in rat.

The superior collicular (SC) cells which project to the intralaminar thalamus (IT; nuclei centralis lateralis, CL; paracentralis, PC; parafascicularis, Pf) in the rat were identified by means of retrograde transport of wheatgerm agglutinin conjugated horseradish peroxidase (WGA-HRP). SC-IT cells were located throughout the mediolateral and rostrocaudal extents of the tectum ipsilateral to the thalamic injection. In this SC, they had a primarily bilaminar distribution in the lower one-half of the stratum griseum intermediale (SGI) and upper portion of the stratum griseum profundum (SGP). In these laminae, SC-IT cells were arranged in clusters or patches similar to those which have been described for many inputs to the deep SC laminae. A small number of SC-IT cells were also observed in the deep laminae of the tectum contralateral to the thalamic injection. Double labelling experiments using True Blue (TB) and Diamidino Yellow (DY) demonstrated that less than 1% of the contralaterally projecting SC-IT cells also innervated ipsilateral IT. Anterograde tracing with [3H]leucine demonstrated further that SC projected heavily to CL, PC and Pf. This projection also extended into the medial portion of the posterior thalamus (PO).

Organization of the intercollicular pathway in rat.

The intercollicular pathway of the rat was studied using autoradiographic (ARG) and horseradish peroxidase (HRP) tracing techniques. The HRP experiments demonstrated that the cells of origin of the intertectal pathway were located primarily in the rostral stratum griseum intermediale ( SGI ), stratum album intermedium (SAI) and stratum griseum profundum (SGP). Intertectal neurons were in most cases multipolar and had average somal diameters which ranged between 8 and 33 micron. Only a small number of superficial layer neurons contributed axons to the intercollicular pathway. ARG tracing showed that the intertectal pathway terminated in the deep layers of the rostral one half of the colliculus. The primary terminal zone was SGP. In addition, labeled axons left this region and coursed dorsally to terminate in a series of patches in the lower SGI and upper SAI. A small number of labeled fibers also reached the stratum opticum (SO) and lower stratum griseum superficiale (SGS).

A wide field electron microscopic analysis of the fiber constituents of the major splanchnic nerve in cat.

The fiber composition of the left major splanchnic nerve was studied in cats by electron microscopy. Comparisons were made between normal and partially degenerated nerve specimens following ventral rhizotomy (T3-L1), or spinal nerve division (T3-L1). Normal, major splanchnic nerves contained 2,500-4,000 myelinated and 10,000-15,000 unmyelinated fibers. Preganglionic fibers included approximately 90% of the finely myelinated (1-7 micrometers) and over 50% of the unmyelinated fibers. Removal of the sensory and preganglionic components by spinal nerve division revealed a third postganglionic fiber category. This included 13-38 small myelinated (1-5 micrometers) and 1,645-7,619 unmyelinated fibers. Finally, a comparison of normal and partially degenerated nerve specimens of both groups (ventral rhizotomy and spinal nerve cut) indicated that splanchnic afferents are made up of virtually all of the 120-350 large myelinated (8-14 micrometers) and 10% of the small myelinated (1-7 micrometers) fibers. A preliminary estimate indicated that about 10-20% of the unmyelinated fibers were sensory. The implications of these findings are discussed.

The organization of visceral sensory neurons in thoracic dorsal root ganglia (DRG) of the cat studied by horseradish peroxidase (HRP) reaction using the cryostat.

The organization of visceral sensory neurons in thoracic dorsal root ganglia (DRG) was studied by retrograde transport of horseradish peroxidase (HRP) from the central cut end of the left major splanchnic nerve of the cat. The majority of HRP-labeled cells were concentrated between T5 and T11. Within a DRG, labeled splanchnic neurons were found in all sectors. There was no consistent pattern of localization within the ganglion although clustering of visceral cell bodies was apparent. It may be that each clustered group of cells innervates individual viscera or reflects a degree of functional segregation.

Segmental organization of sympathetic preganglionic neurons of the splanchnic nerve as revealed by retrograde transport of horseradish peroxidase.

Spinal nerves were transected at selected thoracic levels on the left side and the central cut end of the left major splanchnic nerve was exposed to horseradish peroxidase (HRP) in order to study the preganglionic sympathetic organization in the spinal cord of the cat. In three animals, a total of 4235 HRP labeled neurons were observed (uncorrected counts) in five regions: intermediolateral nucleus (IML) (82.8%), lateral funiculus (LF) (14.7%), intercalatus nucleus (IC) (2.1%), central autonomic (CA) (0.3%) and the anterior horn (AH) (0.1%). The neuronal distribution indicates that sympathetic preganglionic neurons in the thoracic spinal cord are segmentally organized.