Spatial response properties of acoustically responsive neurons in the superior colliculus of the ferret: a map of auditory space

1987 ◽  
Vol 57 (2) ◽  
pp. 596-624 ◽  
Author(s):  
A. J. King ◽  
M. E. Hutchings

Extracellular single-unit recordings were made from auditory neurons in the superior colliculus of ferrets anesthetized with either a neuroleptic or a combination of barbiturate with paralysis. The response properties of these neurons were studied using white-noise bursts presented under free-field conditions in an anechoic chamber. Auditory neurons were found throughout the intermediate and deep layers of the superior colliculus. All neurons were spontaneously active, the rates of discharge varying from 0.1 to 61.1 spikes X s-1. Although the spontaneous discharge interspike-interval histograms for many units approximated to exponential distributions, the histograms of 44% had clear secondary peaks, indicating more than one preferred interval, and could not be modeled by a simple process. Most neurons (50%) responded only at stimulus onset, whereas 12% exhibited sustained discharges and 38% gave onset responses followed by a period of silence or reduced activity and then a period of elevated discharge, which was not apparently related to stimulus offset. Neurons with multipeaked response patterns were concentrated in the stratum griseum profundum. The latencies from arrival of the stimulus at the ear to the onset of neural activity ranged from 6 to 49 ms and decreased with increasing stimulus intensity. Although responsive to sounds over a large region of space, most neurons had clearly defined best positions at which the strongest response was obtained. The response declined as the speaker was moved away from this position, and nearly all units had peaked response profiles. The spatial tuning varied between different neurons, but most were more sharply tuned in elevation than in azimuth. Increasing the stimulus intensity did not, in general, alter the best positions of these neurons, but usually resulted in a broadening of the receptive fields, although other units became more sharply tuned. The best positions of auditory neurons varied systematically in azimuth from 20 degrees into the ipsilateral hemifield to 130 degrees into the contralateral hemifield as the electrode was moved from the rostrolateral to the caudomedial end of the superior colliculus. The best positions shifted in elevation along a rostromedial to caudolateral axis from 60 degrees above to 50 degrees below the visuoaural plane.(ABSTRACT TRUNCATED AT 400 WORDS)

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.


1987 ◽  
Vol 57 (3) ◽  
pp. 688-701 ◽  
Author(s):  
J. C. Middlebrooks

This study explores the mechanisms of auditory spatial tuning in the superior colliculus of the anesthetized cat by correlating spatial tuning within specific regions of space with particular types of binaural interaction. The auditory spatial tuning of units was measured using a movable, broad-band stimulus presented in a free sound field. The contribution of each ear to the response of a unit was identified by acutely plugging one or the other ear. Every unit became largely or entirely unresponsive when a foam-rubber earplug was placed in the ear contralateral to the recording site. Thus, every unit exhibited an excitatory or facilitatory influence from the contralateral ear. A plug placed in the ipsilateral ear had different effects on different units. For half of the units (16/32), an ipsilateral earplug produced increases in the sizes of the units' receptive fields and increases in the magnitudes of their responses to stimuli presented from most locations. Thus, these units exhibited inhibition from the ipsilateral ear. Another class of units (9/32) exhibited ipsilateral facilitation, in that an ipsilateral earplug caused decreases in the sizes of the units' receptive fields and prominent decreases in their response magnitudes. For the remaining units (7/32), an ipsilateral earplug resulted in decreases in the sizes of the units' receptive fields, but produced both decreases in the responses of units to stimuli presented in their best areas and increases in the responses to stimuli presented away from the best areas. Thus these units exhibited mixed facilitatory and inhibitory ipsilateral influences. The influence of an ipsilateral earplug on a unit's response tended to correlate with its spatial tuning. The region of space within which a sound source was most effective in activating a unit was its “best area”. The best areas of units exhibiting ipsilateral inhibition were located furthest peripherally, those of units showing ipsilateral facilitation were located furthest frontally, and the best areas of units showing mixed ipsilateral influences were located in an intermediate area. The frequency tuning of units measured using a free-field tone source also tended to correlate with the locations of their best areas. Half of the units tested (27/54) responded to tones of the sound pressure levels (SPLs) that were used (up to 50 dB SPL).(ABSTRACT TRUNCATED AT 400 WORDS)


2004 ◽  
Vol 92 (4) ◽  
pp. 2083-2092 ◽  
Author(s):  
Ernest E. Kwegyir-Afful ◽  
Asaf Keller

In addition to a primary somatosensory cortex (SI), the cerebral cortex of all mammals contains a second somatosensory area (SII); however, the functions of SII are largely unknown. Our aim was to explore the functions of SII by comparing response properties of whisker-related neurons in this area with their counterparts in the SI. We obtained extracellular unit recordings from narcotized rats, in response to whisker deflections evoked by a piezoelectric device, and compared response properties of SI barrel (layer IV) neurons with those of SII (layers II to VI) neurons. Neurons in both cortical areas have similar response latencies and spontaneous activity levels. However, SI and SII neurons differ in several significant properties. The receptive fields of SII neurons are at least five times as large as those of barrel neurons, and they respond equally strongly to several principal whiskers. The response magnitude of SII neurons is significantly smaller than that of neurons in SI, and SII neurons are more selective for the angle of whisker deflection. Furthermore, whereas in SI fast-spiking (inhibitory) and regular-spiking (excitatory) units have different spontaneous and evoked activity levels and differ in their responses to stimulus onset and offset, SII neurons do not show significant differences in these properties. The response properties of SII neurons suggest that they are driven by thalamic inputs that are part of the paralemniscal system. Thus whisker-related inputs are processed in parallel by a lemniscal system involving SI and a paralemniscal system that processes complimentary aspects of somatosensation.


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.


1994 ◽  
Vol 71 (1) ◽  
pp. 182-194 ◽  
Author(s):  
A. J. King ◽  
D. R. Moore ◽  
M. E. Hutchings

1. We have investigated the role of monaural cues provided by the outer ear in the construction of a map of auditory space in the superior colliculus. Single-unit recordings were made from the superior colliculus of adult ferrets that were deprived of binaural inputs by surgically ablating the ipsilateral cochlea on postnatal day 21 or 24. 2. The spatial response properties of auditory units in the deeper layers of this nucleus were studied using white-noise bursts presented under free-field conditions in an anechoic chamber. The thresholds of the units recorded in the monaural ferrets were not significantly different from those recorded in the superior colliculus of normal adult ferrets. In both groups the unit thresholds varied by 30-50 dB in each region of the superior colliculus. 3. In normal and monaural ferrets the elevation tuning tended to be sharper than the azimuth tuning. At sound levels of approximately 10 dB above threshold the auditory units recorded in both groups of animals were tuned to a specific region of space that was restricted in azimuth and elevation. The spatial location at which the maximum response was obtained (auditory best position) varied topographically in azimuth along the rostrocaudal axis of the nucleus and in elevation along the mediolateral axis. 4. The azimuthal distribution of best positions associated with each recording location in the superior colliculus of the monaural ferrets and the alignment between this dimension of the auditory map and that of the visual map in the overlying superficial layers were no different from those found at corresponding near-threshold sound levels in normal ferrets. 5. Elevation spatial selectivity was examined in a smaller sample of units. Although elevation best positions shifted downward from the medial to the lateral side of the nucleus in both normal and monaural ferrets, we found that the topography of the auditory representation and its alignment with the visual representation were statistically different in the two groups of animals. 6. Increasing the sound level does not affect the representation of auditory space in normal ferrets. However, when the stimulus level presented to monoaural ferrets was increased, the receptive fields either expanded so that the responses were no longer tuned to any particular region of space, or the responses remained tuned but exhibited a marked shift in the value of the best position.(ABSTRACT TRUNCATED AT 400 WORDS)


2006 ◽  
Vol 95 (4) ◽  
pp. 2083-2097 ◽  
Author(s):  
Heather N. Wenk ◽  
Jill-Desiree Brederson ◽  
Christopher N. Honda

Peripherally delivered opiates attenuate mechanical and thermal hyperalgesia in experimental models of inflammation, suggesting that activation of peripheral opioid receptors decreases the excitability of nociceptors in inflamed tissues. The current study examines the effects of peripheral morphine sulfate on response properties of sensory neurons in healthy and inflamed skin. Afferent units (185) were isolated from tibial nerve of rats using an in vitro glabrous skin-nerve teased-fiber preparation. Of these, 107 units were from normal healthy skin, and 78 were from inflamed skin 18 h after intraplantar injection of complete Freund's adjuvant. As a population, C-fiber units innervating inflamed skin exhibited properties characteristic of sensitization when compared with units innervating healthy control skin. Mechanical thresholds were lowered, responses to noxious mechanical and thermal stimuli were elevated, a greater proportion of units was spontaneously active, and the average rate of spontaneous discharge was higher. Response properties in other conduction velocity groups remained unchanged. Fifty-eight percent of C and C/Aδ nociceptors innervating inflamed skin were opiate-sensitive, and their excitability was attenuated by direct application of morphine to their receptive fields. All morphine-sensitive units were nociceptors from inflamed skin with conduction velocities <1.3 m/s. Morphine effects were concentration-dependent and naloxone-sensitive, indicating that the effects were receptor-mediated. These findings provide direct evidence that morphine acts through peripheral opioid receptors to inhibit the activity of cutaneous nociceptors under conditions of inflammation.


2002 ◽  
Vol 87 (5) ◽  
pp. 2602-2611 ◽  
Author(s):  
Robert N. S. Sachdev ◽  
Kenneth C. Catania

Star-nosed moles have an extraordinary mechanosensory system consisting of 22 densely innervated nasal appendages covered with thousands of sensitive touch domes. A single appendage acts as the fovea and the star is constantly shifted to touch this foveal appendage to objects of interest. Here we investigated the receptive fields on the star and the response properties of 144 neurons in the mole's primary somatosensory cortex (S1). Excitatory receptive fields were defined by recording multiunit activity from the S1 representations of the nasal appendages that form the star, while stimulating the touch domes on the skin surface with a small probe. Receptive fields were among the smallest reported for mammalian glabrous skin, averaging <1 mm2. The smallest receptive fields were found for the fovea representation, corresponding to its greater cortical magnification. Single units were then isolated, primarily from the representation of the somatosensory fovea, and the skin surface was stimulated with a small probe attached to a piezoelectric wafer controlled by a computer interface. The response properties of neurons and the locations of inhibitory surrounds were evaluated with two complementary approaches. In the first set of experiments, single microelectrodes were used to isolate unit activity in S1, and data were collected for stimulation to different areas of the sensory star. In the second set of experiments, a multi-electrode array (4 electrodes spaced at 200 μm in a linear sequence) was used to simultaneously record from isolated units in different cortical areas representing different parts of the sensory periphery. These experiments revealed a short-latency excitatory discharge to stimulation of the fovea followed by a long-lasting suppression of spontaneous activity. Sixty-one percent of neurons responded with an excitatory off response at the end of the stimulus; the remaining 39% of cells did not respond or were inhibited at stimulus offset. Stimulation of areas surrounding the central receptive field often revealed inhibitory surrounds. Forty percent of the neurons that responded to mechanosensory stimulation of the receptive field center were inhibited by stimulation of surrounding areas of skin on the same appendage. In contrast to neurons in rodent barrels, few neurons within a stripe representing an appendage responded to stimulation of neighboring (nonprimary) appendages on the snout. The small receptive fields, short latencies, and inhibitory surrounds are consistent with the star's role in rapidly determining the locations and identities of objects in a complex tactile environment.


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