Selected Abstracts of Dr. Frost's Work

A full HTML publication list is available at http://psyc.queensu.ca/~frost/public.html.

1. Troje, N. and Frost, B.J. Head-bobbing in pigeons: How stable is the hold phase? Journal of Experimental Biology, 2000, 203:935-940. (Written up in New Scientist, 165(2227):23).

   Abstract: The head movement of a walking pigeon Columba livia is characterized by two alternating phases, a thrust phase and a hold phase. While the head is rapidly thrust forward during the thrust phase, it has been shown repeatedly that it remains virtually motionless with respect to translation along a horizontal axis (roll axis) during the hold phase. It has been shown that the stabilization during the hold phase is under visual control. This has led to the view that the pigeon's head-bobbing is an optokinetic response to stabilize the retinal image during the hold phase. However, it has never been shown explicitly that the head is really held stable in space with respect to other translatory or rotatory dimensions. Using videography, we show here that this is in fact the case: except for a small but systematic slip that presumably serves as an error signal for retinal image stabilization, the head of the pigeon remains locked in space not only with respect to the horizontal (roll) axis but also with respect to vertical translation (along the yaw axis) and with respect to rotation around the pitch and yaw axes.

2. Sun, H.J. and Frost, B.J. Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons. Nature Neuroscience, 1998, 1, 296-303. (Written up in "News & Views" section 1, 261-263).

   Abstract: Three types of looming selective neurons have been found in the nucleus rotundus of pigeons, each computing a different optical variable related to image expansion of objects approaching on a direct collision course with the bird. None of these neurons respond to simulated approach toward stationary objects. A detailed analysis of the time course of these neurons' firing pattern to approaching objects of different sizes and velocities shows that, one group of neuron signals relative rate of expansion (tau), a second group signals absolute rate of expansion (ROE), and a third group signals yet another optical variable (eta). The parameter is required for the computation of both and , whose respective ecological functions probably provide precise "time-to-collision" information, and "early warning" for large approaching objects.

3. Wylie, D.R., Bischof, W.F. and Frost, B.J. Common reference frame for neural coding of translational and rotational optic flow. Nature,1998, 392(6673):278-82.

   Abstract: Self-movement of an organism through the environment is guided jointly by information provided by the vestibular system and by visual pathways that are specialized for detecting 'optic flow'. Motion of any object through space, including the self-motion of organisms, can be described with reference to six degrees of freedom: rotation about three orthogonal axes, and translation along these axes. Here we describe neurons in the pigeon brain that respond best to optic flow resulting from translation along one of the three orthogonal axes. We show that these translational optic flow neurons, like rotational optic flow neurons, share a common spatial frame of reference with the semicircular canals of the vestibular system. The three axes to which these neurons respond best are the vertical axis and two horizontal axes orientated at 45 degrees to either side of the body midline.

4. van der Willigen, R.F., Frost, B.J. and Wagner, H. Stereoscopic depth perception in the owl. NeuroReport, 1998, 9(6), 1233-1237.

   Abstract: It is unclear whether the neural algorithm that underlies stereoscopic vision in birds incorporates both low level (camouflage breaking) and high level (depth ordering) comparisons of information available to each of the eyes. Both visual functions were successfully tested by examining transitive inference performance in 2 barn owls trained to discriminate static Julesz random dot stereograms, thus demonstrating a capacity to detect relative depth using fine retinal disparity as the sole cue for discrimination. Behavioral tests provide strong evidence that the barn owl possesses global stereopsis comparable to that found in the macaque monkey. The owl's best stereoacuity was 2 min of arc.

5. Sun, H.J. and Frost, B.J. Motion processing in pigeon tectum: equiluminant chromatic mechanisms. Experimental Brain Research, 1997, 116(3):434-44.

   Abstract: Recent psychophysical and neurophysiological studies have suggested that, in mammals, there are interactions between the P (colour processing) and M (motion processing) visual pathways, which were previously believed to be parallel and separate. In this study, the role colour information plays in the coding of object motion was determined in the tectofugal pathway of pigeons. The responses of motion-sensitive neurons in the tectum to moving stimuli formed by chromatic contrast were recorded extracellularly using standard single-unit recording techniques. A moving coloured object was presented on a uniform (opponent coloured) background (e.g. blue-on-yellow, red-on-green and black-on-white). Through systematically manipulation of the luminance contrast between object and background, an equiluminant condition was generated. It was found that, at chromatic equiluminance, the majority of cells maintain some level of response. The mean magnitude of the response at equiluminance was about one-third of the response at maximal contrast to the same chromatic border. These results suggest that tectal units can detect motion of a pattern defined by a pure colour contour, although the strength of output is considerably weaker than that for the movement of patterns formed by luminance contrast.

6. Wylie, D.R.W. and Frost, B.J. The pigeon optokinetic system: Visual input in extraocular muscle coordinates. Visual Neuroscience, 1996, 13, 945-953.

   Abstract: The generation of compensatory eye movements in response to rotational head movements involves the transformation of visual-optokinetic and vestibular signals into commands controlling the appropriate eye muscles. Previously, it has been shown that the three systems (optokinetic, vestibular, and eye muscle) share a similar three-dimensional reference frame. In this report, we suggest that a peculiarity in the structure of the horizontal recti in pigeons demonstrates that the optokinetic system is organized with respect to the eye muscles rather than the vestibular canals. Measurements of the orientation of the plane for each of the lateral and medial recti were obtained. These were compared with the direction preferences of optokinetic neurons responsive to horizontal motion, namely "back" units in the nucleus of the basal optic root (nBOR), "forward" units in the pretectal nucleus lentiformis mesencephali (LM), and "vertical axis" (VA) Purkinje cells in the flocculus. The average direction preference of LM neurons excited in response to forward (temporal to nasal) visual motion, and VA Purkinje cells in response to optokinetic motion in the ipsilateral visual field was approximately parallel to the visual horizontal. This corresponded to the orientation of the medial rectus, which was also approximately parallel to the visual horizontal. The average direction preference of nBOR neurons excited in response to backward (nasal to temporal) visual motion, and VA Purkinje clls in response to optokinetic motion in the contralateral visual field was approximately 20-30 deg down from the visual horizontal. The orientation of the lateral rectus was also approximately 20-30 deg down from the visual horizontal. These data suggest that the incoming optokinetic signals are organized with respect to the outgoing extraocular muscle commands.

7. Wang, S.R., Wang, Y.-C., and Frost, B.J. Differential modulation of visual activity in the pigeon optic tectum by magnocellular and parvocellular components of the nucleus isthmi. Experimental Brain Research., 1995, 104, 376-384.

Abstract: The electrophysiological responses of 162 tectal cells to computer-generated visual stimuli were extracellularly recorded from 24 homing pigeons before and after injecting either lidocaine or N-methyl-D-aspartate (NMDA) into the nucleus isthmi pars magnocellularis (Imc) or the nucleus isthmi pars parvocellularis (Ipc). Micro-injections of lidocaine into Imc resulted in a significant reduction of firing rate in 80% of tectal cells, whose excitatory receptive fields (ERFs) were localized within the ERF of the Imc cell where the lidocaine was injected. In contrast, when lidocaine was injected into Ipc under identical circumstances it had no effect on the visually driven activity of 68% of tectal cells. However, when the excitatory amino acid NMDA was injected into Ipc it produced a significant reduction in the visually driven firing of 75% of tectal neurons when their ERFs were within the isthmic ERF, while similar application of NMDA into Imc had no effect on the visually driven response of 94% of tectal neurons. When the ERFs of tectal cells were localized outside the ERF of the isthmic cell where the chemical was injected, Imc-injected lidocaine had no effect in 9 out of 10 tectal cells, whereas Ipc-injected NMDA increased firing in 7 out of 17 tectal cells. Therefore, it is suggested that the Imc-tectal fibers participate in a positive feedback pathway and the Ipc-tectal fibers are involved in a negative feedback pathway.

8. Wylie, D.R., Shaver, S.W., and Frost B.J. The visual response properties of neurons in the nucleus of the basal optic root of the northern saw-whet owl (Aegolius acadicus). Brain Behaviour and Evolution, 1994, 43(1), 15-25.

   Abstract: The nucleus of the basal optic root (nBOR) in birds is a component of the accessory optic system (AOS) which is involved in the analysis of visual flowfields normally resulting from self-motion. Using standard extracellular techniques, we recorded from 81 single-unit and multi-unit clusters in the nBOR of the northern saw-whet owl, Aegolius acadicus, an avian species that has a visual system with frontal emphasis. These cells responded best to large patterns of random dots moving either upward (52%), downward (31%) or nasal to temporal (N-T; contralateral visual field; 15%). Only 2 units (2%) preferred temporal to nasal motion. 'Up' units were found in the dorsal portion of the nucleus whereas 'Down' units were located more ventrally. The N-T units were found in both the lateral margin of the nucleus and ventral to the Down units in the lateral half of the nucleus. About half of the units tested (10/19) responded to stimulation of the ipsilateral as well as the contralateral eye. For all but one cell, the direction preference of both eyes was the same in visual space. When compared with previous studies of pigeons (Columba livia) and chickens (Gallus domesticus), these findings reveal that the nBOR in all three avian species have important similarities with respect to direction preference and functional compartmentalization. Furthermore, the high proportion of binocular neurons found in the nBOR of the saw-whet owl is similar to the condition generally reported in frontal eyed mammals and hence may reflect adaptation.

9. Wagner H. and Frost B. Disparity-sensitive cells in the owl have a characteristic disparity. Nature, 1993, 364(6440), 796-8.

   Abstract: We experience the visual world as being three-dimensional. A major source of depth information derives from the slightly different views of each eye, leading to small variations in the retinal images ('disparities'). Neurons sensitive to visual disparities are thought to form the neural basis of stereo vision. Barn owls as well as several mammalian species have neurons that are sensitive to visual disparities. But how visual disparities are represented in the brain has been a matter of discussion ever since the first disparity-sensitive neurons were found some 25 years ago. Here we adopt a new approach to this problem and study the neural computation of visual disparities with a paradigm borrowed from auditory research. The measurement of interaural time difference (ITD) has many similarities with the measurement of visual disparity on the formal, algorithmic level. We speculate that the similarities might extend to the level of neural computation. The neural representation of ITD is well understood, and we have studied the representation of disparities with visual stimuli analogous to those successfully used in acoustic experiments. For example, ITD is converted in the brain to a pathlength on an axon that, owing to the finite conduction velocity in neurons, exactly matches the external ITD. This pathlength is called 'characteristic delay'. Our results suggest that there is an analogue of the characteristic delay in stereo vision which we propose to call 'characteristic disparity'.

10. Wylie, D.R., Kripalani, T. and Frost, B.J. Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. I. Functional organization of neurons discriminating between translational and rotational visual flow. Journal of Neurophysiology, 1993, 70(6), 2632-46.

    Abstract: 1. Extracellular recordings were made from 235 neurons in the vestibulocerebellum (VbC), including the flocculus (lateral VbC), nodulus (folium X), and ventral uvula (ventral folium IXc,d), of the anesthetized pigeon, in response to an optokinetic stimulus. 2. The optokinetic stimuli consisted of two black and white random-dot patterns that were back-projected onto two large tangent screens. The screens were oriented parallel to each other and placed on either side of the bird's head. The resultant stimulus covered the central 100 degrees x 100 degrees of each hemifield. The directional tuning characteristics of each unit were assessed by moving the largefield stimulus in 12 different directions, 30 degrees apart. The directional tuning curves were performed monocularly or binocularly. The binocular directional tuning curves were performed with the direction of motion the same in both eyes (in-phase; e.g., ipsi = upward, contra = upward) or with the direction of motion opposite in either eye (antiphase; e.g., ipsi = upward, contra = downward). 3. Mossy fiber units (n = 17) found throughout folia IXa,b and IXc,d had monocular receptive fields and exhibited direction selectivity in response to stimulation of either the ipsilateral (n = 12) or contralateral (n = 5) eye. None had binocular receptive fields. 4. The complex spike (CS) activity of 218 Purkinje cells in folia IXc,d and X exhibited direction selectivity in response to the large-field visual stimulus moving in one or both visual fields. Ninety-one percent of the cells had binocular receptive fields that could be classified into four groups: descent neurons (n = 112) preferred upward motion in both eyes; ascent neurons (n = 14) preferred downward motion in both eyes; roll neurons (n = 33) preferred upward and downward motion in the ipsilateral and contralateral eyes, respectively; and yaw neurons (n = 40) preferred forward and backward motion in the ipsilateral and contralateral eyes, respectively. Within all groups, most neurons (70%) showed an ipsilateral dominance. 5. For most binocular neurons (91%), the maximum depth of modulation occurred with simultaneous stimulation of both eyes, compared with monocular stimulation of the dominant eye alone. For the translation neurons (descent and ascent), binocular inphase stimulation produced the maximum depth of modulation, whereas for the rotation neurons (roll and yaw), binocular antiphase stimulation produced the maximum depth of modulation. 6. There was a clear functional segregation of the translation and rotation neurons.

11. Wylie, D.R. and Frost,B.J. Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. II. The 3-dimensional reference frame of rotation neurons in the flocculus. Journal of Neurophysiology, 1993, 70(6), 2647-59.

    Abstract: 1. The complex spike activity of Purkinje cells in the flocculus in response to rotational flowfields was recorded extracellularly in anesthetized pigeons. 2. The optokinetic stimulus was produced by a rotating "planetarium projector." A light source was placed in the center of a tin cylinder, which was pierced with numerous small holes. A pen motor oscillated the cylinder about its long axis. This apparatus was placed above the bird's head and the resultant rotational flow-field was projected onto screens that surrounded the bird on all four sides. The axis of rotation of the planetarium could be oriented to any position in three-dimensional space. 3. Two types of responses were found: vertical axis (VA; n = 43) neurons responded best to visual rotation about the vertical axis, and H-135i neurons (n = 34) responded best to rotation about a horizontal axis. The preferred orientation of the horizontal axis was at approximately 135 degrees ipsilateral azimuth. VA neurons were excited by rotation about the vertical axis producing forward (temporal to nasal) and backward motion in the ipsilateral and contralateral eyes, respectively, and were inhibited by rotation in the opposite direction. H-135i neurons in the left flocculus were excited by counterclockwise rotation about the 135 degrees ipsilateral horizontal axis and were inhibited by clockwise motion. Thus, the VA and H-135i neurons, respectively, encode visual flowfields resulting from head rotations stimulating the ipsilateral horizontal and ipsilateral anterior semicircular canals. 4. Sixty-seven percent of VA and 80% of H-135i neurons had binocular receptive fields, although for most binocular cells the ipsilateral eye was dominant. Binocular stimulation resulted in a greater depth of modulation than did monocular stimulation of the dominant eye for 69% of the cells. 5. Monocular stimulation of the VA neurons revealed that the best axis for the contralateral eye was tilted back 11 degrees, on average, to the best axis for ipsilateral stimulation. For the H-135i neurons, the best axes for monocular stimulation of the two eyes were approximately the same. 6. By stimulating circumscribed portions of the monocular receptive fields of the H-135i neurons with alternating upward and downward largefield motion, it was revealed that the contralateral receptive fields were bipartite. Upward motion was preferred in the anterior 45 degrees of the contralateral field, and downward motion, was preferred in the central 90 degrees of the contralateral visual field.

12. Telford, L. and Frost, B.J. Factors affecting the onset and magnitude of linear vection. Perception & Psychophysics, 1993, 53(6), 682-92.

    Abstract: The role of central and peripheral vision in the production of linear vection was assessed by using displays in which flow structure and sources of internal and external depth information were manipulated. Radial optical flow was more effective for inducing self-motion in both central and peripheral visual fields than was lamellar flow in displays of the same size. The presence of external occlusion information was necessary to induce linear vection when small displays were composed of lamellar flow, whereas the effectiveness of small radial displays did not depend on the availability of occlusion edges.

13. Wang, Y.C., Jiang, S., and Frost, B.J. Visual processing in pigeon nucleus rotundus: luminance, color, motion, and looming subdivisions. Visual Neuroscience, 1993, 10(1), 21-30.

    Abstract: The responses of single cells to luminance, color and computer-generated spots, bars, kinematograms, and motion-in-depth stimuli were studied in the nucleus rotundus of pigeons. Systematic electrode penetrations revealed that there are several functionally distinct subdivisions within rotundus where six classes of visual-selective cells cluster. Cells in the dorsal-posterior zone of the nucleus respond selectively to motion in depth (i.e. an expanding or contracting figure in the visual field). Most cells recorded from the dorsal-anterior region responded selectively to the color of the stimulus. The firing rate of the cells in the anterior-central zone, however, is dramatically modulated by changing the level of illumination over the whole visual field. Cells in the ventral subdivision strongly respond to moving occlusion edges and very small moving objects, with either excitatory or inhibitory responses. These results indicate that visual information processing of color, ambient illumination, and motion in depth are segregated into different subdivisions at the level of nucleus rotundus in the avian brain.

14. Telford, L., Spratley, J. and Frost, B.J. Linear vection in the central visual field facilitated by kinetic depth cues. Perception, 1992, 21(3), 337-49.

    Abstract: Illusory self-motion (vection) is thought to be determined by motion in the peripheral visual field, whereas stimulation of more central retinal areas results in object-motion perception. Recent data suggest that vection can be produced by stimulation of the central visual field provided it is configured as a more distant surface. In this study vection strength (tracking speed, onset latency, and the percentage of trials where vection was experienced) and the direction of self-motion produced by displays moving in the central visual field were investigated. Apparent depth, introduced by using kinetic occlusion information, influenced vection strength. Central displays perceived to be in the background elicited stronger vection than identical displays appearing in the foreground. Further, increasing the eccentricity of these displays from the central retina diminished vection strength. If the central and peripheral displays were moved in opposite directions, vection strength was unaffected, and the direction of vection was determined by motion of the central display on almost half of the trials when the centre was far. Near centres produced fewer centre-consistent responses. A complete understanding of linear vection requires that factors such as display size, retinal locus, and apparent depth plane are considered.

15. Wang, Y. and Frost, B.J. Time to collision is signalled by neurons in the nucleus rotundus of pigeons. Nature, 1992, 356(6366), 236-8.

    Abstract: Throughout the animal kingdom, the sight of a rapidly approaching object usually signals danger and elicits an escape response. Gibson suggested that the symmetrical expansion of an object's image (looming) is the critical variable determining that the object is on a collision course with the observer. Similarly, large expanding flow-fields like those produced by locomotion may precipitate manoeuvres such as turning or landing. From such observations it has been shown that the optic flow parameter, tau, which specifies time to contact with the approaching object best fits the behavioural data. We describe a subpopulation of neurons in the nucleus rotundus of the pigeon brain that respond selectively to objects moving on a collision course towards the bird.

16. Wang, Y.C. and Frost, B.J. Visual response characteristics of neurons in the nucleus isthmi magnocellularis and nucleus isthmi parvocellularis of pigeons. Experimental Brain Research, 1991, 87(3), 624-33.

    Abstract: The visual response characteristics of single cells in the nucleus isthmi (NI) of pigeons were investigated using standard extracellular recording techniques. The results show that both major components of NI, the parvocellular NI (Ipc) and the magnocellular NI (Imc), have a tight retinotopic organization where nasal regions of the visual field are mapped onto the rostral poles of Ipc and Imc, and temporal regions of the visual field are mapped onto the caudal poles. The more ventral regions of these nuclei receive input from more inferior regions of visual space. The receptive fields (RFs) of both Ipc and Imc are large and oval-shaped, and their long axis is oriented vertically in the visual field. Most RFs are distributed on the contralateral visual horizon, and no binocular responses were found in either Ipc or Imc. All of the excitatory RFs of NI cells were surrounded by large inhibitory regions which participated in the dramatic modulation of the driven visual response when a large background pattern was moved across this zone. Although both Ipc and Imc neurons are driven best by small dark spots, some of them also show orientation selectivity to bars which may result from their oval-shaped RF (74% of Imc cells, 20/38, were orientation selective as compared to 10% of the Ipc cells, 3/30). It is suggested that some tectal cells with small RFs, and which originate from a vertically oriented zone may converge onto a single NI neuron to produce the elliptical shaped receptive fields.

17. Wylie, D.R. and Frost, B.J. Purkinje cells in the vestibulocerebellum of the pigeon respond best to either translational or rotational wholefield visual motion. Experimental Brain Research, 1991, 86(1), 229-32.

    Abstract: Using standard extracellular techniques, the response properties of neurons in the vestibulocerebellum of the pigeon to movement of a wholefield visual stimulus were determined. Complex spike activity of Purkinje cells was modulated in a direction-selective manner by the stimulus and 94% of cells were binocularly driven. Some neurons preferred the same direction of wholefield motion in both eyes, simulating optic flow which results from self-translation, while others preferred the opposite direction in each eye, simulating optic flow resulting from rotation. Four functional classes of neurons were found: (1) Descent cells preferred upward motion in both eyes; (2) Ascent neurons preferred downward motion in both eyes; (3) Roll cells preferred upward and downward motion in the ipsilateral and contralateral eyes respectively; and (4) Yaw cells preferred forward (temporal to nasal) and backward motion in the ipsilateral and contralateral eyes respectively. The observation that these neurons clearly distinguish rotational and translational optic flow patterns suggest they may play an important role in controlling locomotor activities of the pigeon.

Updated December 2004