Effect of spike blockade on the receptive-field size of amacrine and ganglion cells in the rabbit retina

1996 ◽  
Vol 75 (5) ◽  
pp. 1878-1893 ◽  
Author(s):  
S. A. Bloomfield

1. Intracellular recordings were obtained from 21 amacrine cells and 12 ganglion cells in the isolated, superfused retina-eyecup of the rabbit. Cells were subsequently labeled with horseradish peroxidase (HRP) or N-(2-aminoethyl)-biotinamide hydrochloride (Neurobiotin) for morphologic identification. 2. Initial experiments performed on three amacrine cells and three ganglion cells showed that 1 microM tetrodotoxin (TTX) abolished all spiking. This included both large-amplitude and small-amplitude spikes recorded in many amacrine cells, indicating that they are mediated by voltage-gated sodium channels. 3. The center-receptive-field size of 18 amacrine cells and 9 ganglion cells was measured with the use of a 50-microns-wide/6.0-mm-long rectangular slit of light that was displaced along its minor axis (parallel to the visual streak) in steps as small as 3 microns. The retina was then bathed in 1 microM TTX, or individual cells were injected with 50 mM QX-314, a quatemary lidocaine derivative, to abolish all spiking, and the center-receptive field of each cell was then remeasured. 4. Although TTX blocked spiking in all ganglion cells (dendritic diameters ranging from 302 to 969 microns), it produced no significant change in the size of their center-receptive fields. This finding argues that passive, electrotonic spread of synaptic inputs to ganglion cell dendritic arbors is adequate for efficient propagation from terminal branches to the soma; active propagation via voltage-gated sodium channels plays no apparent role. 5. In contrast, TTX and QX-314 had variable effect on the receptive fields of amacrine cells, which was related to the size of their dendritic arbors. Whereas TTX had no significant effect on the receptive-field size of amacrine cells whose dendritic arbors were < 525 microns across, the center-receptive fields of larger amacrine cells were reduced, on average, by 40%; QX-314 produced a very similar average reduction of 39%. Moreover, for these larger cells, there was a direct relationship between the magnitude of the reduction in receptive-field size produced by TTX or QX-314 and the size of a cell's dendritic arbor. This relationship was true whether the change in receptive-field size was measured in absolute terms or as percent reduction from control values. 6. Interestingly, TTX and QX-314 also significantly reduced the amplitude of slow potentials recorded in amacrine cells by an average of 22 and 24%, respectively. However, the amplitude of slow potentials recorded in ganglion cells were relatively uneffected by TTX. 7. These findings are consistent with the idea that, for amacrine cells with dendritic arbors spanning > 525 microns, active propagation of synaptic signals mediated by voltage-gated sodium channels is necessary for efficient movement of information across a cell's dendritic arbor and thus plays a major role in shaping their receptive fields. Although the TTX effects may also reflect an indirect contribution from altered synaptic input derived from presynaptic spiking neurons, the strong similarity between the effects of TTX and QX-314 argues that any such contribution was minor. For smaller amacrine cells, passive, electrotonic spread of signals appears adequate for efficient propagation within their limited dendritic arbors.

2006 ◽  
Vol 23 (1) ◽  
pp. 137-142 ◽  
Author(s):  
WAYNE MICHAEL KING ◽  
VIMAL SARUP ◽  
YVES SAUVÉ ◽  
COLLEEN M. MORELAND ◽  
DAVID O. CARPENTER ◽  
...  

Glaucoma is a major cause of blindness and is characterized by death of retinal ganglion cells. In a rat model of glaucoma in which intraocular pressure is raised by cautery of episcleral veins, the somata and dendritic arbors of surviving retinal ganglion cells expand. To assess physiological consequences of this change, we have measured visual receptive-field size in a primary retinal target, the superior colliculus. Using multiunit recording, receptive-field sizes were measured for glaucomatous eyes and compared to both those measured for contralateral control eyes and to homolateral eyes of unoperated animals. Episcleral vein occlusion increased intraocular pressure. This was accompanied by a significant increase in receptive-field size across the superior colliculus. The expansion of receptive fields was proportional to both degree and duration of the increase of intraocular pressure. We suggest that this increase in the size of receptive fields of glaucomatous eyes may be related to the increase in the size of dendritic arbors of the surviving ganglion cells in retina.


1997 ◽  
Vol 14 (6) ◽  
pp. 1153-1165 ◽  
Author(s):  
Stewart A. Bloomfield ◽  
Daiyan Xin

AbstractRecent studies have shown that amacrine and ganglion cells in the mammalian retina are extensively coupled as revealed by the intercellular movement of the biotinylated tracers biocytin and Neurobiotin. These demonstrations of tracer coupling suggest that electrical networks formed by proximal neurons (i.e. amacrine and ganglion cells) may underlie the lateral propagation of signals across the inner retina. We studied this question by comparing the receptive-field size, dendritic-field size, and extent of tracer coupling of amacrine and ganglion cells in the dark-adapted, supervised, isolated retina eyecup of the rabbit. Our results indicate that while the center-receptive fields of proximal neurons are approximately 15% larger than their corresponding dendritic diameters, this slight difference can be explained by factors other than electrical coupling such as tissue shrinkage associated with histological processing. However, the extent of tracer coupling of amacrine and ganglion cells was, on average, about twice the size of the corresponding receptive fields. Thus, the receptive field of an individual proximal neuron matched far more closely to its dendritic diameter than to the size of the tracer-coupled network of cells to which it belonged. The exception to this rule was the AII amacrine cells for which center-receptive fields were 2–3 times the size of their dendritic diameters but matched closely to the size of the tracer-coupled arrays. Thus, with the exception of AII cells, our data indicate that tracer coupling between proximal neurons is not associated with an enlargement of their receptive fields. Our results, then, provide no evidence for electrical coupling or, at least, indicate that extensive lateral spread of visual signals does not occur in the proximal mammalian retina.


1994 ◽  
Vol 71 (5) ◽  
pp. 1672-1691 ◽  
Author(s):  
S. A. Bloomfield

1. Intracellular recordings were obtained from amacrine and ganglion cells in the isolated, superfused retina-eyecup preparation of the rabbit to test the orientation sensitivity of their responses. Cell identification was based on morphological criteria following injection of horseradish peroxidase (HRP) or N-(2-aminoethyl)-biotinamide hydrochloride (Neurobiotin) to visualize soma-dendritic architectures. 2. In terms of the physiological mechanisms generating their sensitivity, two types of orientation-sensitive amacrine cell and a single type of orientation-sensitive ganglion cell were found. These cell types were termed orientation selective and orientation biased. Cells were subtypes further into on- or off-center receptive-field categories. 3. The receptive fields of orientation-selective amacrine and ganglion cells were composed of two inhibitory fields that flanked the excitatory center receptive field along the preferred orientation. These inhibitory flanks produced a center receptive-field anisotropy with its major axis corresponding to the preferred orientation: either parallel or orthogonal to the visual streak. When a stimulus was oriented orthogonal to the preferred orientation (i.e., at the null orientation), the inhibitory fields were stimulated, resulting in a null inhibition that blocked the center-mediated excitation. Stimulation of these inhibitory flanks was absolutely essential to evoke the orientation selectivity of these cells. The null response reflected inhibition associated with a conductance increase and not disfacilitation. 4. Orientation-biased amacrine cells displayed a center receptive-field anisotropy with its major axis oriented either parallel or orthogonal to the visual streak. These cells preferred light stimuli oriented along the major axis of the center receptive field. However, whereas the excitatory response of these cells was reduced when a stimulus was rotated from the preferred orientation, there was no corresponding hyperpolarization. No null inhibition was detected even after modulation of the membrane potential with extrinsic current. 5. Although orientation-biased amacrine cells were morphologically heterogeneous, they all displayed dendritic arbors that were markedly elongated along an axis corresponding to their physiological preferred orientation. Thus it appears that the elongated dendritic fields of these cells may provide for the anisotropy of their center receptive fields and, in turn, their orientation sensitivity. 6. Orientation-selective amacrine cells formed a rather homogeneous morphological group of cells. These neurons displayed large, radially symmetric dendritic arbors with diameters averaging 1,100 microns. There were no asymmetries in their dendritic fields and thus no clear structural basis for their orientation selectivity. 7. In contrast, orientation-selective ganglion cells displayed diverse soma-dendritic architecture and thus could not be placed into a single morphological class.(ABSTRACT TRUNCATED AT 400 WORDS)


2005 ◽  
Vol 93 (6) ◽  
pp. 3537-3547 ◽  
Author(s):  
Chong Weng ◽  
Chun-I Yeh ◽  
Carl R. Stoelzel ◽  
Jose-Manuel Alonso

Each point in visual space is encoded at the level of the thalamus by a group of neighboring cells with overlapping receptive fields. Here we show that the receptive fields of these cells differ in size and response latency but not at random. We have found that in the cat lateral geniculate nucleus (LGN) the receptive field size and response latency of neighboring neurons are significantly correlated: the larger the receptive field, the faster the response to visual stimuli. This correlation is widespread in LGN. It is found in groups of cells belonging to the same type (e.g., Y cells), and of different types (i.e., X and Y), within a specific layer or across different layers. These results indicate that the inputs from the multiple geniculate afferents that converge onto a cortical cell (approximately 30) are likely to arrive in a sequence determined by the receptive field size of the geniculate afferents. Recent studies have shown that the peak of the spatial frequency tuning of a cortical cell shifts toward higher frequencies as the response progresses in time. Our results are consistent with the idea that these shifts in spatial frequency tuning arise from differences in the response time course of the thalamic inputs.


2021 ◽  
Author(s):  
Miloslav Sedlacek ◽  
William Grimes ◽  
Morgan Musgrove ◽  
Amurta Nath ◽  
Hua Tian ◽  
...  

In retinal neurons, morphology strongly influences visual response features. Ganglion cell (GC) dendrites ramify in distinct strata of the inner plexiform layer (IPL) so that GCs responding to light increments (ON) or decrements (OFF) receive appropriate excitatory inputs. This vertical stratification prescribes response polarity and ensures consistent connectivity between cell types, whereas the lateral extent of GC dendritic arbors typically dictates receptive field (RF) size. Here, we identify circuitry in mouse retina that contradicts these conventions. A2 amacrine cells are interneurons understood to mediate 'cross-over' inhibition by relaying excitatory input from the ON layer to inhibitory outputs in the OFF layer. Ultrastructural and physiological analyses show, however, that some A2s deliver powerful inhibition to OFF GC somas and proximal dendrites in the ON layer, rendering their inhibitory RFs smaller than their dendritic arbors. This OFF pathway, avoiding entirely the OFF region of the IPL, challenges several tenets of retinal circuitry.


1991 ◽  
Vol 6 (3) ◽  
pp. 271-281 ◽  
Author(s):  
S.L. Pallas ◽  
B.L. Finlay

AbstractUnilateral partial ablation of the superior colliculus in the hamster results in a compression of the retinotopic map onto the remaining tectal fragment. In a previous electrophysiological study (Pallas & Finlay, 1989a), we demonstrated that receptive-field properties of single tectal units (including receptive-field size) remain unchanged, despite the increased afferent/target convergence ratios in the compressed tecta. The present study was done to investigate the mechanism that produces increased convergence from retina to tectum at the population level while maintaining apparent stability of convergence at the single neuron level. We injected comparable quantities of horseradish peroxidase into the tecta of normal adult hamsters and adult hamsters that had received neonatal partial tectal ablations of varying magnitude. We then compared the area of retina backfilled from the injection and the number and density of labeled retinal ganglion cells within it to the size of the remaining tectal fragment.As expected from earlier anatomical (Jhaveri & Schneider, 1974) and physiological (Finlay et al., 1979a; Pallas & Finlay, 1989a) studies demonstrating compression of the retinotectal projection, we found that the area of retina labeled from a single tectal injection site increases linearly with decreasing tectal fragment size. However, for fragment sizes down to 30% of normal, total number of retinal ganglion cells projecting to the injection site remains in or above the normal range. For large lesions (less than 30% of tectum remaining), total number of labeled retinal ganglion cells declines from normal, despite the fact that a larger absolute area of retina is represented on each unit of tectum under these conditions. Comparison of retinal ganglion cell density with tectal fragment size shows an initial decline with decreasing fragment size, which becomes sharper with very large lesions (small tectal fragments).The maintenance of the normal number of retinal ganglion cells innervating each patch of tectum could be accomplished by an elimination of the tectal collaterals of some retinal ganglion cells. Our results suggest that, in addition to collateral elimination, reduction in the size of ganglion cell arbors is occurring, since the peak density of backfilled ganglion cells declines less rapidly than backfilled retinal area increases, especially for small lesions. However, arbor reduction and collateral elimination must occur in such a way that individual tectal cells represent the same amount of visual space as normal.Thus, collateral elimination and arbor reduction are two mechanisms that operate to maintain afferent/target convergence ratios (and thus receptive-field properties) over large variations in afferent availability. This compensation may occur through an activity-dependent stabilization mechanism that does not change its selectivity even when excess afferents are available. For very large lesion sizes, receptive-field size and innervating ganglion cell number and density are not preserved, thus demonstrating a limit to the afferent/target matching mechanism. The same ontogenetic mechanisms might provide a buffer for normal variations in afferent populations, and could help to align topographic maps with differing numbers of afferents.


2014 ◽  
Vol 112 (10) ◽  
pp. 2529-2544 ◽  
Author(s):  
Dylan F. Cooke ◽  
Adam B. Goldring ◽  
Mary K. L. Baldwin ◽  
Gregg H. Recanzone ◽  
Arnold Chen ◽  
...  

Somatosensory processing in the anesthetized macaque monkey was examined by reversibly deactivating posterior parietal areas 5L and 7b and motor/premotor cortex (M1/PM) with microfluidic thermal regulators developed by our laboratories. We examined changes in receptive field size and configuration for neurons in areas 1 and 2 that occurred during and after cooling deactivation. Together the deactivated fields and areas 1 and 2 form part of a network for reaching and grasping in human and nonhuman primates. Cooling area 7b had a dramatic effect on receptive field size for neurons in areas 1 and 2, while cooling area 5 had moderate effects and cooling M1/PM had little effect. Specifically, cooling discrete locations in 7b resulted in expansions of the receptive fields for neurons in areas 1 and 2 that were greater in magnitude and occurred in a higher proportion of sites than similar changes evoked by cooling the other fields. At some sites, the neural receptive field returned to the precooling configuration within 5–22 min of rewarming, but at other sites changes in receptive fields persisted. These results indicate that there are profound top-down influences on sensory processing of early cortical areas in the somatosensory cortex.


2004 ◽  
Vol 91 (4) ◽  
pp. 1510-1515 ◽  
Author(s):  
Elena Timofeeva ◽  
Philippe Lavallée ◽  
Dominique Arsenault ◽  
Martin Deschênes

This study addresses the origins of multiwhisker-receptive fields of neurons in the thalamic ventral posterior medial (VPM) nucleus of the rat. We sought to determine whether multiwhisker-receptive field synthesis occurs in VPM through convergent projections from the principalis (PrV) and interpolaris (SpVi) nuclei, or in PrV by intersubnuclear projections from the spinal trigeminal complex. We tested these hypotheses by recording whisker-evoked responses in PrV and VPM before and after electrolytic lesion of the SpVi in lightly anesthetized rats. Before the lesion PrV cells responded, on average, to 3.2 ± 1.2 whiskers but responsiveness was reduced to 1.07 ± 0.31 whisker after the lesion. A similar reduction of receptive field size was observed in VPM, where neurons responded, on average, to 2.94 ± 0.95 whiskers before the lesion and to 1.05 ± 0.22 whisker after the lesion. Thus one can conclude that intersubnuclear projections mediate surround whisker-receptive fields in PrV, and therefore in VPM. However, it has previously been shown that parasagittal brain stem transection, which severed ascending projections from SpVi, but left intersubnuclear connections intact, rendered VPM cells monowhisker responsive. We wondered whether midline brain stem lesion modified receptive field properties in SpVi. In normal rats SpVi cells responded, on average, to 7.52 ± 4.25 whiskers, but responsiveness was dramatically reduced to 1.47 ± 1.07 whisker after the lesion. Together these results indicate that the synthesis of surround receptive fields in subcortical stations relies almost exclusively on intersubnuclear projections from the spinal trigeminal complex to the PrV.


1998 ◽  
Vol 80 (1) ◽  
pp. 120-129 ◽  
Author(s):  
Robert W. Dykes ◽  
A. D. Craig

Dykes, Robert W. and A. D. Craig. Control of size and excitability of mechanosensory receptive fields in dorsal column nuclei by homolateral dorsal horn neurons. J. Neurophysiol. 80: 120–129 1998. Both accidental and experimental lesions of the spinal cord suggest that neuronal processes occurring in the spinal cord modify the relay of information through the dorsal column-lemniscal pathway. How such interactions might occur has not been adequately explained. To address this issue, the receptive fields of mechanosensory neurons of the dorsal column nuclei were studied before and after manipulation of the spinal dorsal horn. After either a cervical or lumbar laminectomy and exposure of the dorsal column nuclei in anesthetized cats, the representation of the hindlimb or of the forelimb was defined by multiunit recordings in both the dorsal column nuclei and in the ipsilateral spinal cord. Next, a single cell was isolated in the dorsal column nuclei, and its receptive field carefully defined. Each cell could be activated by light mechanical stimuli from a well-defined cutaneous receptive field. Generally the adequate stimulus was movement of a few hairs or rapid skin indentation. Subsequently a pipette containing either lidocaine or cobalt chloride was lowered into the ipsilateral dorsal horn at the site in the somatosensory representation in the spinal cord corresponding to the receptive field of the neuron isolated in the dorsal column nuclei. Injection of several hundred nanoliters of either lidocaine or cobalt chloride into the dorsal horn produced an enlargement of the receptive field of the neuron being studied in the dorsal column nuclei. The experiment was repeated 16 times, and receptive field enlargements of 147–563% were observed in 15 cases. These data suggest that the dorsal horn exerts a tonic inhibitory control on the mechanosensory signals relayed through the dorsal column-lemniscal pathway. Because published data from other laboratories have shown that receptive field size is controlled by signals arising from the skin, we infer that the control of neuronal excitability, receptive field size and location for lemniscal neurons is determined by tonic afferent activity that is relayed through a synapse in the dorsal horn. This influence of dorsal horn neurons on the relay of mechanosensory information through the lemniscal pathways must modify our traditional views concerning the relative independence of these two systems.


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