Prenatal development of the receptive fields of individual trigeminal ganglion cells in the rat

1993 ◽  
Vol 69 (4) ◽  
pp. 1171-1180 ◽  
Author(s):  
N. L. Chiaia ◽  
W. R. Bauer ◽  
R. W. Rhoades

1. Extracellular single-unit recording and receptive-field mapping techniques were used to evaluate the response characteristics of trigeminal (V) ganglion cells in unanesthetized, decerebrate, fetal rats between the ages of embryonic (E-) day 15 and E-20 (E-0 is the day of conception). 2. The receptive-field properties of the cells (n = 282) recorded at all of these ages except E-15 were remarkably similar; V primary afferents were generally silent in the absence of peripheral stimulation (94.3%) and gave rapidly adapting responses to innocuous tactile stimuli (97.5%). Rapid response decrements to repeated stimuli were observed in 9 of the 14 cells (64%) tested. 3. None of the cells recorded were activated by either heat or cold. No attempt was made to evaluate responses to noxious mechanical stimuli. 4. Particular attention was paid to neurons whose receptive fields involved mystacial vibrissae follicles. At all ages, neurons were recorded that responded to indentation of the skin at the base of the vibrissae, but vibrissa deflection was not an adequate stimulus for any of the cells tested. At all ages, nearly all (89.0%) of the 127 cells with vibrissa-related receptive fields responded to indentation of one and only one follicle. 5. These results indicate that the response properties (e.g., adaptation characteristics, ability to respond to repeated stimuli) of V primary afferents in fetal rats differ substantially from those of V ganglion cells in adult animals, but that the receptive-field size for these neurons in prenatal rats is, with very rare exceptions, adult-like from the earliest age at which they can be recorded. 6. These results, when considered together with the results of previous retrograde tracing experiments in fetal animals, suggest that the initial projections of V primary afferents to their peripheral targets may be quite accurate.

1996 ◽  
Vol 75 (6) ◽  
pp. 2441-2450 ◽  
Author(s):  
D. D. Rasmusson

1. Single neurons in the ventroposterior lateral thalamic nucleus were studied in 10 anesthetized raccoons, 4 of which had undergone amputation of the fourth digit 4-5 mo before recording. Neurons with receptive fields on the glabrous skin of a forepaw digit were examined in response to electrical stimulation of the “on-focus” digit that contained the neuron's receptive field and stimulation of an adjacent, “off-focus” digit. 2. In normal raccoons all neurons responded to on-focus stimulation with an excitation at a short latency (mean 13 ms), whereas only 63% of the neurons responded to off-focus digit stimulation. The off-focus responses had a longer latency (mean 27.2 ms) and a higher threshold than the on-focus responses (800 and 452 microA, respectively). Only 3 of 32 neurons tested with off-focus stimulation had both a latency and a threshold within the range of on-focus values. Inhibition following the excitation was seen in the majority of neurons with both types of stimulation. 3. In the raccoons with digit removal, the region of the thalamus that had lost its major peripheral input (the “deafferented” region) was distinguished from the normal third and fifth digit regions on the basis of the sequence of neuronal receptive fields within a penetration and receptive field size as described previously. 4. Almost all of the neurons in the deafferented region (91%) were excited by stimulation of one or both adjacent digits. The average latency for these responses was shorter (15.3 ms) and the threshold was lower than was the case with off-focus stimulation in control animals. These values were not significantly different from the responses to on-focus stimulation in the animals with digit amputation. 5. These results confirm that reorganization of sensory pathways can be observed at the thalamic level. In addition to the changes in the somatotopic map that have been shown previously with the use of mechanical stimuli, the present paper demonstrates an improvement in several quantitative measures of single-unit responses. Many of these changes suggest that this reorganization could be explained by an increased effectiveness of preexisting, weak connections from the off-focus digits; however, the increase in the proportion of neurons responding to stimulation of adjacent digits may indicate that sprouting of new connections also occurs.


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.


1997 ◽  
Vol 78 (4) ◽  
pp. 2048-2060 ◽  
Author(s):  
Steven H. Devries ◽  
Denis A. Baylor

DeVries, Steven H. and Denis A. Baylor. Mosaic arrangement of ganglion cell receptive fields in rabbit retina. J. Neurophysiol. 78: 2048–2060, 1997. The arrangement of ganglion cell receptive fields on the retinal surface should constrain several properties of vision, including spatial resolution. Anatomic and physiological studies on the mammalian retina have shown that the receptive fields of several types of ganglion cells tile the retinal surface, with the degree of receptive field overlap apparently being similar for the different classes. It has been difficult to test the generality of this arrangement, however, because it is hard to sample many receptive fields in the same preparation with conventional single-unit recording. In our experiments, the response properties and receptive fields of up to 80 neighboring ganglion cells in the isolated rabbit retina were characterized simultaneously by recording with a multielectrode array. The cells were divided into 11 classes on the basis of their characteristic light responses and the temporal structures of their impulse trains. The mosaic arrangement of receptive fields for cells of a given class was examined after the spatial profile of each receptive field was fitted with a generalized Gaussian surface. For eight cell classes the mosaic arrangement was similar: the profiles of neighboring cells approached each other at the 1-σ border. Thus field centers were 2 σ apart. The layout of fields for the remaining three classes was not well characterized because the fields were poorly fitted by a single Gaussian or because the cells responded selectively to movement. The 2-σ center-center spacing may be a general principle of functional organization that minimizes spatial aliasing and confers a uniform spatial sensitivity on the ganglion cell population.


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.


2021 ◽  
Vol 15 ◽  
Author(s):  
Hui Chen ◽  
Hong-Ping Xu ◽  
Ping Wang ◽  
Ning Tian

It was well documented that both the size of the dendritic field and receptive field of retinal ganglion cells (RGCs) are developmentally regulated in the mammalian retina, and visual stimulation is required for the maturation of the dendritic and receptive fields of mouse RGCs. However, it is not clear whether the developmental changes of the RGC receptive field correlate with the dendritic field and whether visual stimulation regulates the maturation of the dendritic field and receptive field of RGCs in a correlated manner. The present work demonstrated that both the dendritic and receptive fields of RGCs continuously develop after eye opening. However, the correlation between the developmental changes in the receptive field size and the dendritic field varies among different RGC types. These results suggest a continuous change of synaptic converging of RGC synaptic inputs in an RGC type-dependent manner. Besides, light deprivation impairs both the development of dendritic and receptive fields.


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.


1993 ◽  
Vol 90 (23) ◽  
pp. 11142-11146 ◽  
Author(s):  
S Bisti ◽  
C Trimarchi

Prenatal unilateral enucleation in mammals causes an extensive anatomical reorganization of visual pathways. The remaining eye innervates the entire extent of visual subcortical and cortical areas. Electrophysiological recordings have shown that the retino-geniculate connections are retinotopically organized and geniculate neurones have normal receptive field properties. In area 17 all neurons respond to stimulation of the remaining eye and retinotopy, orientation columns, and direction selectivity are maintained. The only detectable change is a reduction in receptive field size. Are these changes reflected in the visual behavior? We studied visual performance in cats unilaterally enucleated 3 weeks before birth (gestational age at enucleation, 39-42 days). We tested behaviorally the development of visual acuity and, in the adult, the extension of the visual field and the contrast sensitivity. We found no difference between prenatal monocularly enucleated cats and controls in their ability to orient to targets in different positions of the visual field or in their visual acuity (at any age). The major difference between enucleated and control animals was in contrast sensitivity:prenatal enucleated cats present a loss in sensitivity for gratings of low spatial frequency (below 0.5 cycle per degree) as well as a slight increase in sensitivity at middle frequencies. We conclude that prenatal unilateral enucleation causes a selective change in the spatial performance of the remaining eye. We suggest that this change is the result of a reduction in the number of neurones with large receptive fields, possibly due to a severe impairment of the Y system.


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.


1994 ◽  
Vol 11 (4) ◽  
pp. 703-720 ◽  
Author(s):  
Ming Sun ◽  
A. B. Bonds

AbstractThe two-dimensional organization of receptive fields (RFs) of 44 cells in the cat visual cortex and four cells from the cat LGN was measured by stimulation with either dots or bars of light. The light bars were presented in different positions and orientations centered on the RFs. The RFs found were arbitrarily divided into four general types: Punctate, resembling DOG filters (11%); those resembling Gabor filters (9%); elongate (36%); and multipeaked-type (44%). Elongate RFs, usually found in simple cells, could show more than one excitatory band or bifurcation of excitatory regions. Although regions inhibitory to a given stimulus transition (e.g. ON) often coincided with regions excitatory to the opposite transition (e.g. OFF), this was by no means the rule. Measurements were highly repeatable and stable over periods of at least 1 h. A comparison between measurements made with dots and with bars showed reasonable matches in about 40% of the cases. In general, bar-based measurements revealed larger RFs with more structure, especially with respect to inhibitory regions. Inactivation of lower cortical layers (V-VI) by local GABA injection was found to reduce sharpness of detail and to increase both receptive-field size and noise in upper layer cells, suggesting vertically organized RF mechanisms. Across the population, some cells bore close resemblance to theoretically proposed filters, while others had a complexity that was clearly not generalizable, to the extent that they seemed more suited to detection of specific structures. We would speculate that the broadly varying forms of cat cortical receptive fields result from developmental processes akin to those that form ocular-dominance columns, but on a smaller scale.


1983 ◽  
Vol 50 (6) ◽  
pp. 1479-1496 ◽  
Author(s):  
D. R. Kenshalo ◽  
O. Isensee

Recordings were made from single SI cortical neurons in the anesthetized macaque monkey. Each isolated cortical neuron was tested for responses to a standard series of mechanical stimuli. The stimuli included brushing the skin, pressure, and pinch. The majority of cortical neurons responded with the greatest discharge frequency to brushing the receptive field, but neurons were found in areas 3b and 1 that responded maximally to pinching the receptive field. A total of 68 cortical nociceptive neurons were examined in 10 animals. Cortical neurons that responded maximally to pinching the skin were also tested for responses to graded noxious heat pulses (from 35 to 43, 45, 47, and 50 degrees C). If the neuron failed to respond or only responded to 50 degrees C, the receptive field was also heated to temperatures of 53 and 55 degrees C. Fifty-six of the total population of nociceptive neurons were tested for responses to the complete series of noxious heat pulses: 46 (80%) exhibited a progressive increase in the discharge frequency as a function of stimulus intensity, and the spontaneous activity of two (4%) was inhibited. One population of cortical nociceptive neurons possessed restricted, contralateral receptive fields. These cells encoded the intensity of noxious mechanical and thermal stimulation. Sensitization of primary afferent nociceptors was reflected in the responses of SI cortical nociceptive neurons when the ascending series of noxious thermal stimulation was repeated. The population of cortical nociceptive neurons with restricted receptive fields exhibited no adaptation in the response during noxious heat pulses of 47 and 50 degrees C. At higher temperatures the response often continued to increase during the stimulus. The other population of cortical nociceptive neurons was found to have restricted, low-threshold receptive fields on the contralateral hindlimb and, in addition, could be activated only by intense pinching or noxious thermal stimuli delivered on any portion of the body. The stimulus-response functions obtained from noxious thermal stimulation of the contralateral hindlimb were not different from cortical nociceptive neurons with small receptive fields. However, nociceptive neurons with large receptive fields exhibited a consistent adaptation during a noxious heat pulse of 47 and 50 degrees C. Based on the response characteristics of these two populations of cortical nociceptive neurons, we conclude that neurons with small receptive fields possess the ability to provide information about the localization, the intensity, and the temporal attributes of a noxious stimulus.4+.


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