Laminar profile of visual response properties in ferret superior colliculus

2013 ◽  
Vol 110 (6) ◽  
pp. 1333-1345 ◽  
Author(s):  
Iain Stitt ◽  
Edgar Galindo-Leon ◽  
Florian Pieper ◽  
Gerhard Engler ◽  
Andreas K. Engel

In the superior colliculus (SC), visual afferent inputs from various sources converge in a highly organized way such that all layers form topographically aligned representations of contralateral external space. Despite this anatomical organization, it remains unclear how the layer-specific termination of different visual input pathways is reflected in the nature of visual response properties and their distribution across layers. To uncover the physiological correlates underlying the laminar organization of the SC, we recorded multiunit and local field potential activity simultaneously from all layers with dual-shank multichannel linear probes. We found that the location of spatial receptive fields was strongly conserved across all visual responsive layers. There was a tendency for receptive field size to increase with depth in the SC, with superficial receptive fields significantly smaller than deep receptive fields. Additionally, superficial layers responded significantly faster than deeper layers to flash stimulation. In some recordings, flash-evoked responses were characterized by the presence of gamma oscillatory activity (40–60 Hz) in multiunit and field potential signals, which was strongest in retinorecipient layers. While SC neurons tended to respond only weakly to full-field drifting gratings, we observed very similar oscillatory responses to the offset of grating stimuli, suggesting gamma oscillations are produced following light offset. Oscillatory spiking activity was highly correlated between horizontally distributed neurons within these layers, with oscillations temporally locked to the stimulus. Together, visual response properties provide physiological evidence reflecting the laminar-specific termination of visual afferent pathways in the SC, most notably characterized by the oscillatory entrainment of superficial neurons.

1997 ◽  
Vol 78 (5) ◽  
pp. 2732-2741 ◽  
Author(s):  
M. T. Wallace ◽  
J. G. McHaffie ◽  
B. E. Stein

Wallace M. T., J. G. McHaffie, and B. E. Stein. Visual response properties and visuotopic representation in the newborn monkey superior colliculus. J. Neurophysiol. 78: 2732–2741, 1997. Visually responsive neurons were recorded in the superior colliculus (SC) of the newborn rhesus monkey. The receptive fields of these neurons were larger than those in the adult, but already were organized into a well-ordered map of visual space that was very much like that seen in mature animals. This included a marked expansion of the representation of the central 10° of the visual field and a systematic foveal to peripheral increase in receptive field size. Although newborn SC neurons had longer response latencies than did their adult counterparts, they responded vigorously to visual stimuli and exhibited many visual response properties that are characteristic of the adult. These included surround inhibition, within-field spatial summation, within-field spatial inhibition, binocularity, and an adult-like ocular dominance distribution. As in the adult, SC neurons in the newborn preferred a moving visual stimulus and had adult-like selectivities for stimulus speed. The developmentally advanced state of the functional circuitry of the newborn monkey SC contrasts with the comparative immaturity of neurons in its visual cortex. It also contrasts with observations on the state of maturation of the newborn SC in other developmental models (e.g., cat). The observation that extensive visual experience is not necessary for the development of many adult-like SC response properties in the monkey SC may help explain the substantial visual capabilities shown by primates soon after birth.


1981 ◽  
Vol 45 (3) ◽  
pp. 397-416 ◽  
Author(s):  
J. F. Baker ◽  
S. E. Petersen ◽  
W. T. Newsome ◽  
J. M. Allman

1. The response properties of 354 single neurons in the medial (M), dorsomedial (DM), dorsolateral (DL), and middle temporal (MT) visual areas were studied quantitatively with bar, spot, and random-dot stimuli in chronically implanted owl monkeys with fixed gaze. 2. A directionality index was computed to compare the responses to stimuli in the optimal direction with the responses to the opposing direction of movement. The greater the difference between opposing directions, the higher the index. MT cells had much higher direction indices to moving bars than cells in DL, DM, and M. 3. A tuning index was computed for each cell to compare the responses to bars moving in the optimal direction, or flashed in the optimal orientation, with the responses in other directions or orientations within +/- 90 degrees. Cells in all four areas were more sharply tuned to the orientation of stationary flashed bars than to moving bars, although a few cells (9/92( were unresponsive in the absence of movement. DM cells tended to be more sharply tuned to moving bars than cells in the other areas. 4. Directionality in DM, DL, and MT was relatively unaffected by the use of single-spot stimuli instead of bars; tuning in all four areas was broader to spots than bars. 5. Moving arrays of randomly spaced spots were more strongly excitatory than bar stimuli for many neurons in MT (16/31 cells). These random-dot stimuli were also effective in M, but evoked no response or weak responses from most cells in DM and DL. 6. The best velocities of movement were usually in the range of 10-100 degrees/s, although a few cells (22/227), primarily in MT (14/69 cells), preferred higher velocities. 7. Receptive fields of neurons in all four areas were much larger than striate receptive fields. Eccentricity was positively correlated with receptive-field size (r = 0.62), but was not correlated with directionality index, tuning index, or best velocity. 8. The results support the hypothesis that there are specializations of function among the cortical visual areas.


1989 ◽  
Vol 3 (3) ◽  
pp. 249-265 ◽  
Author(s):  
Helen Sherk

AbstractThe existence of multiple areas of extrastriate visual cortex raises the question of how the response properties of each area are derived from its visual input. This question was investigated for one such area in the cat, referred to here as the Clare-Bishop area (Hubel & Wiesel, 1969); it is the region of lateral suprasylvian cortex that receives input from area 17. A novel approach was used, in which kainic acid was injected locally into the Clare-Bishop area, making it possible to record directly from afferent inputs.The response properties of the great majority of a sample of 424 presumed afferents resembled cells in areas 17 and 18. Thus, a systematic comparison was made with cells from area 17's upper layers, the source of its projection to the Clare-Bishop area (Gilbert & Kelly, 1975), to see whether these afferents had distinctive properties that might distinguish them from cells projecting to areas 18 or 19. Some differences did emerge: (1) The smallest receptive fields typical of area 17 were relatively scarce among afferents. (2) Direction-selective afferents were more abundant than were such cells in area 17. (3) End-stopped afferents were extremely rare, although end-stopped cells were common in area 17's upper layers.Despite these differences, afferents were far more similar in their properties to cells in areas 17 and 18 than to cells in the Clare-Bishop area. Compared to the latter, afferents showed major discrepancies in receptive-field size, in direction selectivity, in end-stopping, and in ocular dominance distribution. These differences seem most likely to stem from circuitry intrinsic to the Clare-Bishop area.


1979 ◽  
Vol 42 (6) ◽  
pp. 1640-1655 ◽  
Author(s):  
H. Sherk

1. The visual-response properties of single cells in the cat's superior colliculus and parabigeminal nucleus were compared. In the colliculus, 151 cells (restricted to the upper layer) were studied, and in the parabigeminal nucleus, 134 cells. 2. Response characteristics in the two structures were similar in many respects: among these were receptive-field size, ocular dominance, and lack of specificity for stimulus shape and contrast (light versus dark). 3. Quantitatively, there were some significant differences between the two populations of cells. Parabigeminal neurons tended to respond more brisky and reliably, while being less selective for those stimulus parameters tested (size, velocity, and direction of movement). Spontaneous activity was much higher in the parabigeminal nucleus than in the colliculus. Finally, parabigeminal cell responses to stationary stimuli were somewhat brisker than those of tectal cells. 4. These data suggest that a physiologically distinct population of tectal cells sends input to the parabigeminal nucleus, probably with some convergence on individual cells.


1983 ◽  
Vol 49 (3) ◽  
pp. 674-685 ◽  
Author(s):  
L. Z. Wise ◽  
D. R. Irvine

1. The auditory responses of 207 single neurons in the intermediate and deep layers of the superior colliculus (SC) of barbiturate -or chloralose-anesthetized cats were recorded extracellularly. Sealed stimulating systems incorporating calibrated probe microphone assemblies were employed to present tone- and noise-burst stimuli. 2. All acoustically activated neurons responded with onset responses to noise bursts. Of those neurons also tested with tonal stimuli, approximately 30% were unresponsive over the frequency range tested (0.1-40 kHz), while the others had higher thresholds to tones than to noise. 3. Details of frequency responsiveness were obtained for 55 neurons; 21 were broadly tuned, while 34 were sharply tuned with clearly defined characteristic frequencies (CFs). All sharply tuned neurons had CFs greater than or equal to 10 kHz. 4. The majority of neurons (81%) responded with latencies in the range 8-20 ms; only 11% of neurons had latencies greater than 30 ms. 5. Binaural response properties were examined for 165 neurons. The great majority (79%) received monaural excitatory input only from the contralateral ear (EO). However, most EO cells were binaurally influenced, the contralateral response being either inhibited (EO/I; 96 of 131 units) or facilitated (EO/F; 33 of 131 units) by simultaneous ipsilateral stimulation. Small subgroups were monaurally excited by either ear (EE cells; 8%) or were unresponsive monaurally but responded strongly to binaural stimulation (OO/F cells; 7%). 6. EO/I, EO/F, and OO/F neurons showed characteristic forms of sensitivity to interaural intensity differences (IIDs). The IID functions of EO/I neurons would be expected to produce large contralateral spatial receptive fields with clearly defined medial borders, such as have been described in studies of deep SC neurons employing free-field stimuli. 7. Preliminary evidence suggests a possible topographic organization of IID sensitivity in deep SC, such that the steeply sloping portion of the function (corresponding to the medial edge of the receptive field) is shifted laterally for EO/I neurons located more caudally in the nucleus. 8. The auditory properties of deep SC neurons are compared with previous reports and implications for the organization of auditory input are considered. The binaural properties and auditory spatial fields of deep SC neurons suggest that any representation of auditory space in this structure is unlikely to be based on restricted spatial fields.


1993 ◽  
Vol 70 (3) ◽  
pp. 1115-1136 ◽  
Author(s):  
H. R. Rodman ◽  
S. P. Scalaidhe ◽  
C. G. Gross

1. Inferior temporal cortex (IT) is a "high-order" region of primate temporal visual cortex implicated in visual pattern perception and recognition. To gain some insight into the development of this area, we compared the properties of single neurons in IT in infant monkeys ranging from 5 wk to 7 mo of age with those of neurons in IT in adult animals. Both anesthetized and awake behaving paradigms were used. 2. In immobilized infant monkeys under nitrous oxide anesthesia, the incidence of visually responsive cells was markedly less than in adult monkeys studied under similar conditions. In infants 4-7 mo of age, only half of IT neurons studied were visually responsive, compared with > 80% in adult monkeys. In monkeys < 4 mo old, even fewer (< 10%) could be visually driven. "Habituation" of IT cells to repeated stimulus presentation appeared more pronounced in infant monkeys under nitrous oxide anesthesia than in adult animals. 3. IT cells in the anesthetized infant monkeys that did respond showed receptive field properties similar to those of responsive adult IT neurons studied under similar conditions. Two thirds of the receptive fields plotted in the anesthetized 4 to 7-mo-old group were bilateral, and median field size did not differ between the infants and comparable adult groups, being approximately 20 degrees on a side in each case. 4. In contrast to the results obtained under anesthesia, most IT cells in alert infant monkeys 5 wk-7 mo of age (80%) were responsive to visual stimuli, and this incidence of visually responsive IT neurons did not differ from that obtained in awake adult macaques. However, response magnitude, measured as spikes per second above baseline rate, was significantly lower in the infant alert sample than in the adult control (5.2 vs. 12.6 spikes/s, mean +/- SE, deviation from spontaneous rate, respectively). 5. In addition to having lower magnitudes of visual response, IT cells in the awake infants also tended to have longer and more variable latencies. The overall mean for the infant cells was 196 ms, compared with an overall mean of 140 ms for IT neurons in the alert control adult. 6. Although the magnitude of response of neurons in alert infant IT cortex was lower overall, the incidence and features of stimulus selectivity shown by alert infant IT neurons were strikingly similar to those of IT cells of both anesthetized and unanesthetized adult monkeys.(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 60 (6) ◽  
pp. 2037-2054 ◽  
Author(s):  
R. E. Soodak ◽  
J. I. Simpson

1. The response properties of accessory optic system (AOS) neurons were assessed using single-unit extracellular recording from each of the three AOS terminal nuclei [medial, lateral, and dorsal terminal nuclei (MTN, LTN, and DTN)] in the anesthetized rabbit. 2. AOS neurons had large, monocular (contralateral) receptive fields (tens of degrees on a side) and exhibited a pronounced selectivity to the speed and direction of movement of large, textured patterns. The greatest responses occurred at slow speeds on the order of 0.5 degrees/s. 3. MTN and LTN neurons responded best to movement in near vertical directions. However, the stimulus directions corresponding to the greatest excitation and the greatest inhibition both had a posterior component and, thus, the preferred excitatory and inhibitory directions were not opposite each other. DTN neurons responded most strongly to horizontal movement and were excited by temporal to nasal movement. 4. AOS neurons were unresponsive to natural vestibular stimulation presented as sinusoidal oscillations of the rabbit about the yaw, pitch, and roll axes. 5. The response properties of AOS neurons are remarkably similar to those of the ON, direction-selective ganglion cells of the rabbit retina, and therefore this class of ganglion cell is most likely the predominant, if not the only, direct retinal input to the AOS. The local direction-selective properties of AOS neurons can be accounted for by combining the tuning curves of ON, direction-selective ganglion cells in a simple manner. 6. The low speed preference of AOS neurons, along with their large receptive fields suggests that they are suited to complement the vestibular system in detecting self-motion.


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