Macaque V1 activity during natural vision: effects of natural scenes and saccades

In the present study, we examined the way that scene complexity and saccades combine to sculpt the temporal response patterns of V1 neurons. To bridge the gap between conventional and free viewing experiments, we compared responses of neurons across four paradigms ranging from less to more natural. An optimal bar stimulus was either flashed into a receptive field (RF) or brought into it via saccade and was embedded in either a natural scene or a uniform gray background. Responses to a flashed bar tended to be higher with a uniform rather than natural background. The most novel result reported here is that responses evoked by stimuli brought into the RF via saccades were enhanced compared with the same stimuli flashed during steady fixation. No single factor appears to account entirely for this surprising effect, but there were small contributions from fixational saccades and residual activity carried over from the previous fixation. We also found a negative correlation with cells' response "history" in that a larger response on one fixation was associated with a lower response on the subsequent fixation. The effects of the natural background and saccades exhibited a significant nonlinear interaction with the suppressive effects of the natural background less for stimuli entering RFs with saccades. Together, these results suggest that even responses to standard optimal stimuli are difficult to predict under conditions similar to natural vision, and further demonstrate the importance of naturalistic experimental paradigms to the study of visual processing in V1.     

Independent components of color natural scenes resemble V1 neurons in their spatial and color tuning

It has been hypothesized that mammalian sensory systems are efficient because they reduce the redundancy of natural sensory input. If correct, this theory could unify our understanding of sensory coding; here, we test its predictions for color coding in the primate primary visual cortex (V1). We apply independent component analysis (ICA) to simulated cone responses to natural scenes, obtaining a set of colored independent component (IC) filters that form a redundancy-reducing visual code. We compare IC filters with physiologically measured V1 neurons, and find great spatial similarity between IC filters and V1 simple cells. On cursory inspection, there is little chromatic similarity; however, we find that many apparent differences result from biases in the physiological measurements and ICA analysis. After correcting these biases, we find that the chromatic tuning of IC filters does indeed resemble the population of V1 neurons, supporting the redundancy-reduction hypothesis.     

Responses of V1 neurons to two-dimensional hermite functions

Neurons in primary visual cortex are widely considered to be oriented filters or energy detectors that perform one-dimensional feature analysis. The main deviations from this picture are generally thought to include gain controls and modulatory influences. Here we investigate receptive field (RF) properties of single neurons with localized two-dimensional stimuli, the two-dimensional Hermite functions (TDHs). TDHs can be grouped into distinct complete orthonormal bases that are matched in contrast energy, spatial extent, and spatial frequency content but differ in two-dimensional form, and thus can be used to probe spatially specific nonlinearities. Here we use two such bases: Cartesian TDHs, which resemble vignetted gratings and checkerboards, and polar TDHs, which resemble vignetted annuli and dartboards. Of 63 isolated units, 51 responded to TDH stimuli. In 37/51 units, we found significant differences in overall response size (21/51) or apparent RF shape (28/51) that depended on which basis set was used. Because of the properties of the TDH stimuli, these findings are inconsistent with simple feedforward nonlinearities and with many variants of energy models. Rather, they imply the presence of nonlinearities that are not local in either space or spatial frequency. Units showing these differences were present to a similar degree in cat and monkey, in simple and complex cells, and in supragranular, infragranular, and granular layers. We thus find a widely distributed neurophysiological substrate for two-dimensional spatial analysis at the earliest stages of cortical processing. Moreover, the population pattern of tuning to TDH functions suggests that V1 neurons sample not only orientations, but a larger space of two-dimensional form, in an even-handed manner.     

Responses of cat vestibular neurons to sinusoidal roll tilt

Summary Extracellular recordings were made in the lateral and inferior vestibular nuclei of decerebrate, unanesthetized cats. The firing patterns of single units were studied using small amplitude sinusoidal roll tilts of from 0.01 Hz to 1.0 Hz. Three-fourths of the tilt-sensitive units showed greater modulation of their firing rates as the frequency of the sinusoidal tilt was increased. The responses of cells in both nuclei were similar. These responses were virtually unchanged in cats with chronically plugged semicircular canals, indicating a probable otolith origin for the dynamics of the tilt response.Supported in part by grant NS 02619 from the National Institutes of Health.I wish to thank Vivienne Leon, Barbara Rothar and Susan Wong for their valuable technical assistance. I am especially grateful to Barry Peterson and Victor Wilson for their advice, criticisms and guidance.     

Responses to contour features in macaque area V4

The ventral pathway in visual cortex is responsible for the perception of shape. Area V4 is an important intermediate stage in this pathway, and provides the major input to the final stages in inferotemporal cortex. The role of V4 in processing shape information is not yet clear. We studied V4 responses to contour features (angles and curves), which many theorists have proposed as intermediate shape primitives. We used a large parametric set of contour features to test the responses of 152 V4 cells in two awake macaque monkeys. Most cells responded better to contour features than to edges or bars, and about one-third exhibited systematic tuning for contour features. In particular, many cells were selective for contour feature orientation, responding to angles and curves pointing in a particular direction. There was a strong bias toward convex (as opposed to concave) features, implying a neural basis for the well-known perceptual dominance of convexity. Our results suggest that V4 processes information about contour features as a step toward complex shape recognition.     

Responses to moving slits by single units in cat striate cortex

Summary A quantitative study has been made of the responses to moving slit stimuli by single units in the cat striate cortex whose receptive fields lay within 5° of the visual axis. Special attention was given to finding the optimal stimulus parameters including slit width, length, orientation and speed. The analysis was largely based on averaged response vs. time histograms. Using the classification of simple and complex responses types, the units were further subdivided on the basis of the number of modes in the response and on the presence or absence of directional selectivity. Simple unimodal units with directional selectivity (SUDS) had the most specific stimulus requirements and nearly always had zero background activity. Complex units usually had a high level of background activity. SUDS units also showed a preference for horizontally- and vertically ****-orientated stimuli. Whenever the response survived reversal of contrast the directional selectivity remained independent of the change. Optimal stimulus speeds varied widely from unit to unit with a mean at 4°/sec: simple bimodal units and complex units tended to have higher optimal stimulus speeds and responded over a wider range of speeds than did simple unimodal units. While SUDS units with very small receptive fields tended to prefer slowly moving stimuli, in general there was no correlation between receptive field size and optimal stimulus speed.Selby Fellow of the Australian Academy of Sciences.     

Purified natural and recombinant Fel d 1 and cat albumin in in vitro diagnostics for cat allergy

BACKGROUND: Current diagnostics and therapeutics for cat allergy are based on cat epithelial extracts originating from highly variable source materials. This gives rise to several problems: variability of allergen composition, contamination with house dust mite allergens, and potential transfer of pathogenic agents. OBJECTIVE: The aim of this study was to investigate the feasibility of replacing cat epithelial extracts with purified natural or recombinant allergens. METHODS: Sera (n = 509) were selected on the basis of a positive cat RAST result and tested in a RAST for IgE reactivity to purified Fel d 1, cat albumin (CA), or both. The analysis was performed with both natural and recombinant allergens. In addition, some sera were further analyzed by means of immunoblotting. A serum pool was used for cat RAST inhibition with purified natural and recombinant allergens as inhibitors. RESULTS: Natural and recombinant Fel d 1 caused very similar results: 94.1% and 96.1% positive test results, respectively. In general, the negative sera were low responders to cat extract. The addition of CA (16.7% positive sera) resulted in a decrease in the number of discrepencies between purified allergens and whole extract to 2.8%. Only for 2% of all sera, sensitization to cat was largely explained by IgE reactivity to CA. IgE reactivity to Fel d 1 accounts for 88% of the total IgE response to cat allergens, as was demonstrated by RAST, with Fel d 1 concentrations nearing saturation. Recombinant Fel d 1 performed equally well in the RAST analysis. Recombinant CA was succesfully expressed in the yeast Pichia pastoris, and its immune reactivity closely resembled that of its natural counterpart. CONCLUSION: Natural and recombinant Fel d 1 and CA are good candidates for replacing ill-defined cat dander extracts in diagnostics for cat allergy. Although CA is not essential for the vast majority of cat-sensitized patients, some subjects are selectively sensitized to this serum protein.     

Selectively attending to natural scenes after alcohol consumption: an ERP analysis

Alcohol effects on cognitive, emotional and behavioral processes have been linked to an impairment of attention. Because attention operates at the level of specific cognitive subsystems, recent studies demonstrated alcohol effects in specific post-perceptual processes such as response selection and working memory. Measuring event-related potentials, the present study focused on perceptual processes by utilizing a categorization task where participants had to decide whether briefly presented images contained an animal or not. Findings demonstrate an early differential ERP activity for target compared to non-target images, which was reduced after alcohol intoxication. Thus, alcohol intoxication had deleterious effects at the perceptual level of processing considered to reflect the interaction of top-down (category-related) and bottom-up (stimulus-driven) processes. In addition, post-perceptual processes were also impaired by alcohol intoxication.     

Responses of neurons in primary auditory cortex (A1) to pure tones in the halothane-anesthetized cat

The responses of primary auditory cortex (A1) neurons to pure tones in anesthetized animals are usually described as having mostly narrow, unimodal frequency tuning and phasic responses. Thus A1 neurons are believed not to carry much information about pure tones beyond sound onset. In awake cats, however, tuning may be wider and responses may have substantially longer duration. Here we analyze frequency-response areas (FRAs) and temporal-response patterns of 1,828 units in A1 of halothane-anesthetized cats. Tuning was generally wide: the total bandwidth at 40 dB above threshold was 4 octaves on average. FRA shapes were highly variable and many were diffuse, not fitting into standard classification schemes. Analyzing the temporal patterns of the largest responses of each unit revealed that only 9% of the units had pure onset responses. About 40% of the units had sustained responses throughout stimulus duration (115 ms) and 13% of the units had significant and informative responses lasting 300 ms and more after stimulus offset. We conclude that under halothane anesthesia, neural responses show many of the characteristics of awake responses. Furthermore, A1 units maintain sensory information in their activity not only throughout sound presentation but also for hundreds of milliseconds after stimulus offset, thus possibly playing a role in sensory memory.     

Responses of interneurons in the cat cervical cord to vestibular tilt stimulation

The responses of interneurons in the cervical spinal cord of the decerebrate cat to whole-body tilt were studied with a goal of identifying spinal elements in the production of forelimb vestibular postural reflexes. Interneurons both in the cervical enlargement and at higher levels, from which propriospinal neurons have been identified, were examined, both in animals with intact labyrinths and in animals with nonfunctional semicircular canals (canal plugged). Most cervical interneurons responding to tilt respond best to rotations in vertical planes aligned within 30 degrees of the roll plane. Two to three times as many neurons are excited by side-up roll tilt as are excited by side-down roll. In cats with intact labyrinths, most responses have dynamics proportional either to (and in phase with) the position of the animal or to a sum of position and tilt velocity. This is consistent with input from both otolith organs and semicircular canals. In animals without functioning canals, the "velocity" response is absent. In a few cells (8 out of 76), a more complex response, characterized by an increasing gain and progressive phase lag, was observed. These response dynamics characterize the forelimb reflex in canal-plugged cats and have been previously observed in vestibular neurons in such preparations.     

Responses of neurons in the cat primary auditory cortex to sequential sounds

In the natural acoustic environment sounds frequently arrive at the two ears in quick succession. The responses of a cortical neuron to acoustic stimuli can be dramatically altered, usually suppressed, by a preceding sound. The purpose of this study was to determine if the binaural interaction evoked by a preceding sound is involved in subsequent suppressive interactions observed in auditory cortex neurons. Responses of neurons in the primary auditory cortex (AI) exhibiting binaural suppressive interactions (EO/I) were studied in barbiturate-anesthetized cats. For the majority (72.5%) of EO/I neurons studied, the response to a monaural contralateral stimulus was suppressed by a preceding monaural contralateral stimulus, but was not changed by a preceding monaural ipsilateral stimulus. For this subset of EO/I neurons, when a monaural contralateral stimulus was preceded by a binaural stimulus, the level of both the ipsilateral and the contralateral component of the binaural stimulus influenced the response to the subsequent monaural contralateral stimulus. When the contralateral level of the binaural stimulus was constant, increasing its ipsilateral level decreased the suppression of the response to the subsequent monaural contralateral stimulus. When the ipsilateral level of the binaural stimulus was constant, increasing its contralateral level increased the suppression of the response to the subsequent monaural contralateral stimulus. These results demonstrate that the sequential inhibition of responses of AI neurons is a function of the product of a preceding binaural interaction. The magnitude of the response to the contralateral stimulus is related to, but not determined by the magnitude of the response to the preceding binaural stimulus. Possible mechanisms of this sequential interaction are discussed.     

Responses of cerebellar units to a passive movement in the decerebrate cat

Summary The responses of mossy fibers (MF), granular cells (GrC) and Purkinje cells (PC) were recorded in the cerebellum of the decerebrate cat during a passive movement about the forepaw wrist joint. Three main discharge patterns containing information about all the static and dynamic parameters of the movement were found. Simultaneous recording of complex spikes (CS) and simple spikes (SS) showed that the activity of PC can be modulated through either MF or CF input channels alone or both together. In the latter case SS and CS discharge most commonly showed an opposite behavior, in which the increase of the frequency of one type of spike was accompanied by a decrease of the frequency of the other type. Both inputs displayed tonic and phasic characteristics and all the qualitative discharge patterns observed. Therefore it was concluded that aside from differences in the discharge frequency, both inputs are able to directly signal peripheral events.     

Responses of a spino-olivo-cerebellar pathway in the cat

1. Surface potentials, similar to those found by earlier workers, have been recorded from the vermis of the anterior lobe of the cerebellum following stimulation of muscular, cutaneous and articular nerves of the ipsilateral hind limb. The most conspicuous component of the response consisted of a positive potential succeeded by a smaller negative potential.

2. Micro-electrode recordings showed that this component coincided both with climbing fibre responses in individual Purkinje cells, and with extracellular field potentials within the cerebellar cortex which closely resembled those found by Eccles, Llinás & Sasaki (1966) following electrical stimulation of the inferior olive.

3. Stimulation of the cerebellar surface, in the region where the responses to limb nerve stimulation were largest, led to antidromic invasion of neurones of the contralateral inferior olive. The antidromic action potentials were sometimes followed by up to three orthodromic spikes. Histological techniques were used to show that these neurones were located in the caudal parts of the dorsal and medial accessory olives.

4. Stimulation of nerves of the hind limb evoked discharges of the same neurones of the dorsal accessory olive which were antidromically invaded from the vermis of the anterior lobe. The nerves used (quadriceps, gastrocnemius-soleus, sural and the posterior nerve to the knee joint) were shown to excite heavily overlapping populations of neurones.

5. Those neurones of the medial accessory olive, which were identified antidromically from the anterior lobe vermis, were not discharged by stimulation of hind limb nerves.

6. Simultaneous recording from the surface of the anterior lobe and from the dorsal accessory olive showed that the onset of olive cell discharges occurred about 5 msec before the onset of the positive potential at the cerebellar surface.

     

Relationship between contrast adaptation and orientation tuning in V1 and V2 of cat visual cortex

Previous studies investigating the response properties of neurons in the primary visual cortex of cats and primates have shown that prolonged exposure to optimally oriented, high-contrast gratings leads to a reduction in responsiveness to subsequently presented test stimuli. We recorded from 119 neurons in cat V1 and V2 and found that in a high proportion of cells contrast adaptation also occurs for gratings oriented orthogonal to a neuron's preferred orientation, even though this stimulus did not elicit significant increases in spiking activity. Approximately 20% of neurons adapted equally to all orientations tested and a further 46% showed at least some adaptation to orthogonally oriented gratings, whereas 20% of neurons did not adapt to orthogonal gratings. The magnitude of contrast adaptation was positively correlated with adapting contrast, but was not related to the spiking activity of the cells. Highly direction selective neurons produced stronger adaptation to orthogonally oriented gratings than other neurons. Orientation-related adaptation was correlated with the rate of change of orientation tuning in consecutive cells along electrode penetrations that traveled parallel to the cortical layers. Nonoriented adaptation was most common in areas where orientation preference changed rapidly, whereas orientation-selective adaptation was most common in areas where orientation preference changed slowly. A minority of neurons did not show contrast adaptation (14%). No major differences were found between units in different cortical layers, V1 and V2, or between complex and simple cells. The relevance of these findings to the current understanding of adaptation within the context of orientation column architecture is discussed.     

Local correlation-based circuitry can account for responses to multi-grating stimuli in a model of cat V1

In cortical simple cells of cat striate cortex, the response to a visual stimulus of the preferred orientation is partially suppressed by simultaneous presentation of a stimulus at the orthogonal orientation, an effect known as "cross-orientation inhibition." It has been argued that this is due to the presence of inhibitory connections between cells tuned for different orientations, but intracellular studies suggest that simple cells receive inhibitory input primarily from cells with similar orientation tuning. Furthermore, response suppression can be elicited by a variety of nonpreferred stimuli at all orientations. Here we study a model circuit that was presented previously to address many aspects of simple cell orientation tuning, which is based on local intracortical connectivity between cells of similar orientation tuning. We show that this model circuit can account for many aspects of cross-orientation inhibition and, more generally, of response suppression by nonpreferred stimuli and of other nonlinear properties of responses to stimulation with multiple gratings.     

Responses of cat prepositus hypoglossi neurons to horizontal angular acceleration.

Responses of single cells in the nucleus prepositus hypoglossi following natural stimulation of the horizontal semicircular canals were studied in cats anesthetized with Ketamine hydrochloride. Prepositus hypoglossi neurons were typically silent or low firing at rest and often showed saccadic-like burst or pause activity. During rotation, type I, II, III and IV vestibular responses were observed in the proportions 26, 70, 2.4 and 1.6%, respectively. Type I and II responses were graded as a function of stimulus intensity, exhibited response null points similar to peripheral horizontal canal neurons and had thresholds and gradients which were comparable, in magnitude, to cells in the vestibular nucleus. Some time constant asymmetries were noted during constant angular acceleration which were enhanced with increasing levels of acceleration and were particularly apparent in cells which had a vestibular evoked nystagmic-like modulation in rate. Sinusoidal acceleration responses were low-skew and consistently modulated (in phase and gain) on a cycle-to-cycle basis despite the asymmetries in time-domain time constants and the occasional saccadic or nystagmic-like activity. Phase-lags between peak unitary discharge and head acceleration for type II prepositus hypoglossi neurons were shifted (by ca. 10–20°) towards larger values at each frequency when compared to type I prepositus hypoglossi neurons or to type I neurons in the vestibular nuclei.These results demonstrate that the nucleus prepositus hypoglossi receives a powerful input from both horizontal canals, and its response is qualitatively similar to cells in the vestibular nuclei. At the quantitative level, however, sufficient differences exist between these two neuronal populations which, when combined with the existing electrophysiological evidence, strongly suggest that the prepositus hypoglossi may be involved in a more complex processing of vestibulo-ocular information.     

Responses of isolated Golgi tendon organs of cat to sinusoidal stretch

1. Receptor potential and tension have been recorded from isolated Golgi tendon organs in response to sinusoidal stretch. Responses depended on amplitude and frequency of stretch and on the initial (resting) tension of the preparation. 2. Both tension and receptor potential behaved as power functions of stretch amplitude over most of the range corresponding to physiological tendon strains. However, for very small stretch amplitudes (less than 8 microns), a more linear response was seen. Those characteristics of responses that depended on stretch amplitude behaved similarly at all frequencies examined. 3. Frequency dependence of tension was slight. Its character, a gradual monotonic increase in response with increasing stretch frequency and a constant phase lead of a few degrees, did not change over the examined frequency range from 0.12 to 80 Hz. In contrast, receptor potential displayed a marked frequency dependence, increasing rapidly with increasing frequency of stretch in the range from approximately 1 to 20 Hz, then slowly declining as frequency was further increased. 4. Changes in initial tension of the preparation produced marked parallel changes in the amplitude dependence of tension and receptor potential. Frequency response was not significantly affected. 5. By comparing tension and receptor potential responses, the relative contributions of mechanical and electrical properties of the receptor to the sensory transduction process was examined. The present results suggest that in tendon organs the observed nonlinear dependence on amplitude of stretch originates primarily in the mechanical stage of transduction. Dynamic sensitivity, however, seems largely attributable to ionic processes within the sensory terminal membranes.     

Responses of cat motor cortex neurons to cortico-cortical and somatosensory inputs

Summary Intracellular techniques were used to investigate a cortico-cortical path from sensory cortex to motor cortex of cats. Cortico-cortical epsps were evoked in motor cortex neurons by microstimulation of area 3a. Epsps with latencies between 1.2 and 2.4 ms were identified as monosynaptic. These short latency cortico-cortical effects were recorded in layers II through VI of the motor cortex. Neurons with monosynaptic cortico-cortical epsps also received excitatory inputs from forelimb nerves, usually from both muscle and cutaneous afferent fibers. The epsps evoked from forelimb nerves in motor cortex neurons were preceded by neural activity in somatosensory cortex. Time delays between arrival of inputs in sensory cortex and in motor cortex were compared to the latencies of cortico-cortical epsps in the same motor cortex neurons. It was apparent that the timing was appropriate for the identified cortico-cortical path to have relayed some sensory inputs to motor cortex.Supported by the Medical Research Council of Canada (MT-7373, DG-186), the Harry Botterell Foundation for the Neurological Sciences, the Ontario Ministry of Health, and the Faculty of Medicine, Queen's UniversityRecipient of a Medical Research Council of Canada Studentship.Recipient of a Medical Research Council of Canada Fellowship