Response Properties of Optic Flow Neurons in the Accessory Optic System of Hummingbirds vs. Zebra Finches and Pigeons

Author(s):  
Andrea H Gaede ◽  
Vikram B Baliga ◽  
Graham Smyth ◽  
Cristian Gutiérrez-Ibáñez ◽  
Douglas Leonard Altshuler ◽  
...  

Optokinetic responses function to maintain retinal image stabilization by minimizing optic flow that occurs during self-motion. The hovering ability of hummingbirds is an extreme example of this behaviour. Optokinetic responses are mediated by direction-selective neurons with large receptive fields in the accessory optic system (AOS) and pretectum. Recent studies in hummingbirds showed that, compared to other bird species, (i) the pretectal nucleus lentiformis mesencephali (LM) is hypertrophied, (ii) LM has a unique distribution of direction preferences, and (iii) LM neurons are more tightly tuned to stimulus velocity. In this study, we sought to determine if there are concomitant changes in the nucleus of the basal optic root (nBOR) of the AOS. We recorded the visual response properties of nBOR neurons to largefield drifting random dot patterns and sine wave gratings in Anna's hummingbirds and zebra finches and compared these with archival data from pigeons. We found no differences with respect to the distribution of direction preferences: Neurons responsive to upwards, downwards and nasal-to-temporal motion were equally represented in all three species, and neurons responsive to temporal-to-nasal motion were rare or absent (<5%). Compared to zebra finches and pigeons, however, hummingbird nBOR neurons were more tightly tuned to stimulus velocity of random dot stimuli. Moreover, in response to drifting gratings, hummingbird nBOR neurons are more tightly tuned in the spatio-temporal domain. These results, in combination with specialization in LM, supports a hypothesis that hummingbirds have evolved to be "optic flow specialist" to cope with the optomotor demands of sustained hovering flight.

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.


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.


2000 ◽  
Vol 84 (5) ◽  
pp. 2529-2540 ◽  
Author(s):  
Douglas R. W. Wylie ◽  
Nathan A. Crowder

Neurons in the pretectal nucleus lentiformis mesencephali (LM) are involved in the analysis of optic flow that results from self-motion. Previous studies have shown that LM neurons have large receptive fields in the contralateral eye, are excited in response to largefield stimuli moving in a particular (preferred) direction, and are inhibited in response to motion in the opposite (anti-preferred) direction. We investigated the responses of LM neurons to sine wave gratings of varying spatial and temporal frequency drifting in the preferred and anti-preferred directions. The LM neurons fell into two categories. “Fast” neurons were maximally excited by gratings of low spatial [0.03–0.25 cycles/° (cpd)] and mid-high temporal frequencies (0.5–16 Hz). “Slow” neurons were maximally excited by gratings of high spatial (0.35–2 cpd) and low-mid temporal frequencies (0.125–2 Hz). Of the slow neurons, all but one preferred forward (temporal to nasal) motion. The fast group included neurons that preferred forward, backward, upward, and downward motion. For most cells (81%), the spatial and temporal frequency that elicited maximal excitation to motion in the preferred direction did not coincide with the spatial and temporal frequency that elicited maximal inhibition to gratings moving in the anti-preferred direction. With respect to motion in the anti-preferred direction, a substantial proportion of the LM neurons (32%) showed bi-directional responses. That is, the spatiotemporal plots contained domains of excitation in addition to the region of inhibition. Neurons tuned to stimulus velocity across different spatial frequency were rare (5%), but some neurons (39%) were tuned to temporal frequency. These results are discussed in relation to previous studies of the responses of neurons in the accessory optic system and pretectum to drifting gratings and other largefield stimuli.


1993 ◽  
Vol 69 (4) ◽  
pp. 1314-1322 ◽  
Author(s):  
T. X. Fan ◽  
A. F. Rosenberg ◽  
M. Ariel

1. Single units were recorded extracellularly in the turtle's cerebellar cortex from an isolated brain preparation during visual stimulation. Only a small fraction of the isolated units responded to visual stimuli. For these visually responsive units, the most effective visual stimulus was a moving check pattern that covered the entire surface of the retinal eyecup. The visually responsive units had little or no spontaneous spike activity, nor were they driven by flashes of diffuse light or stationary patterns. 2. All the visually responsive units were direction sensitive and were driven exclusively by the contralateral eye. This direction tuning was well fit by a limacon model (mean correlation coefficient, 0.89). The distribution of the entire sample indicates a slight preponderance of upward preferred directions. 3. The direction tuning of these cerebellar units was independent of stimulus contrast or the pattern's configuration (such as checkerboards or random check or dot patterns). In the preferred direction, a unit's spike frequency increased monotonically as a function of stimulus velocity until approximately 10 degrees/s, but remained direction sensitive (relative to the opposite direction) at speeds as fast as 100 degrees/s. 4. In some experiments the ventrocaudal brain stem was transected in the frontal plane just caudal to the cerebellar peduncles. Although this lesion presumably removes climbing fiber input from the inferior olivary nuclei, the visual-response properties in the cerebellar cortex were unaffected. 5. The response properties of these units indicate that they encode retinal slip information in the cerebellum.(ABSTRACT TRUNCATED AT 250 WORDS)


2001 ◽  
Vol 85 (5) ◽  
pp. 2111-2129 ◽  
Author(s):  
Jonathan B. Levitt ◽  
Robert A. Schumer ◽  
S. Murray Sherman ◽  
Peter D. Spear ◽  
J. Anthony Movshon

It is now well appreciated that parallel retino-geniculo-cortical pathways exist in the monkey as in the cat, the species in which parallel visual pathways were first and most thoroughly documented. What remains unclear is precisely how many separate pathways pass through the parvo- and magnocellular divisions of the macaque lateral geniculate nucleus (LGN), what relationships—homologous or otherwise—these pathways have to the cat's X, Y, and W pathways, and whether these are affected by visual deprivation. To address these issues of classification and trans-species comparison, we used achromatic stimuli to obtain an extensive set of quantitative measurements of receptive field properties in the parvo- and magnocellular laminae of the LGN of nine macaque monkeys: four normally reared and five monocularly deprived of vision by lid suture near the time of birth. In agreement with previous studies, we find that on average magnocellular neurons differ from parvocellular neurons by having shorter response latencies to optic chiasm stimulation, greater sensitivity to luminance contrast, and better temporal resolution. Magnocellular laminae are also distinguished by containing neurons that summate luminance over their receptive fields nonlinearly (Y cells) and whose temporal response phases decrease with increasing stimulus contrast (indicative of a contrast gain control mechanism). We found little evidence for major differences between magno- and parvocellular neurons on the basis of most spatial parameters except that at any eccentricity, the neurons with the smallest receptive field centers tended to be parvocellular. All parameters were distributed unimodally and continuously through the parvo- and magnocellular populations, giving no indications of subpopulations within each division. Monocular deprivation led to clear anatomical effects: cells in deprived-eye laminae were pale and shrunken compared with those in nondeprived eye laminae, and Cat-301 immunoreactivity in deprived laminae was essentially uniformly abolished. However, deprivation had only subtle effects on the response properties of LGN neurons. Neurons driven by the deprived eye in both magno- and parvocellular laminae had lower nonlinearity indices (i.e., summed signals across their receptive fields more linearly) and were somewhat less responsive. In magnocellular laminae driven by the deprived eye, neuronal response latencies to stimulation of the optic chiasm were slightly shorter than those in the nondeprived laminae, and receptive field surrounds were a bit stronger. No other response parameters were affected by deprivation, and there was no evidence for loss of a specific cell class as in the cat.


1988 ◽  
Vol 60 (6) ◽  
pp. 2055-2072 ◽  
Author(s):  
J. I. Simpson ◽  
C. S. Leonard ◽  
R. E. Soodak

1. To compare the spatial organization of the direction selectivity of neurons in the medial terminal nucleus (MTN) of the accessory optic system with that of neurons in the adjacent ventral tegmentum, extracellular single-unit recordings were made in the anesthetized rabbit. The ventral tegmental neurons were located in a region called the visual tegmental relay zone (VTRZ), which is defined by the ventral tegmental terminal field of contralaterally projecting MTN neurons. 2. Some of the present sample of MTN neurons (5 of 34) had monocular receptive fields composed of two parts distinguished by a marked difference in the orientation of their respective direction-selective tuning curves. For one part of the receptive field the preferred excitatory direction was "up," while for the other part it was "down." Such receptive fields for one eye were called bipartite, whereas the more usually encountered MTN receptive fields, which could be characterized by a single direction-selective tuning curve, were called uniform. 3. Of the 16 neurons recorded from the VTRZ, all but one were binocular. For these neurons, both uniform and bipartite receptive fields were found for each eye alone. The only monocular neuron encountered in the VTRZ had a contralateral, bipartite receptive field. 4. The spatial organization of the direction selectivity of bipartite receptive fields strongly suggests that they are suited to represent rotation of the visual field about a horizontal axis located in the vertical plane that divides the receptive field into two parts. 5. The boundary between the two parts of the bipartite receptive fields was found using handheld visual stimuli at one of two azimuthal locations, either close to 45 degrees or between 95 and 125 degrees (the 0 degree reference was rostral in the midsagittal plane). This particular structure of the bipartite receptive fields suggests that their preferred rotation axes have a close spatial relation to the best-response axes of the semicircular canals. 6. Seven VTRZ neurons were antidromically activated by electrical stimulation of the ipsilateral dorsal cap of the inferior olive. Since the receptive fields of VTRZ neurons have many of the structural features characteristic of the receptive fields of rostral dorsal cap neurons we conclude that the spatial organization of the receptive fields of dorsal cap neurons is, for the most part, synthesized prior to the inferior olive.(ABSTRACT TRUNCATED AT 400 WORDS)


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.


1996 ◽  
Vol 13 (2) ◽  
pp. 375-383 ◽  
Author(s):  
Alexander F. Rosenberg ◽  
Michael Ariel

AbstractThe turtle's optokinetic response is described by a simple model that incorporates visual-response properties of neurons in the pretectum and accessory optic system. Using data from neuronal and eye-movement recordings that have been previously published, the model was realized using algebraic-block simulation software. It was found that the optokinetic response, modelled as a simple negative feedback system, was similar to that measured from a behaving animal. Because the responses of retinal-slip detecting neurons corresponded to the nonlinear, closed-loop optokinetic response, it was concluded that the visual signals encoded in these neurons could provide sufficient sensory information to drive the optokinetic reflex. Furthermore, it appears that the low gain of optokinetic eye movements in turtles, which have a negligible velocity storage time constant, may allow stable oculomotor output in spite of neuronal delays in the reflex pathway. This model illustrates how visual neurons in the pretectum and accessory optic system can contribute to visually guided eye movements.


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