A. B. Bonds

Classifying simple and complex cells on the basis of response modulation

Hubel and Wiesel (1962; Journal of Physiology, London, 160, 106-154) introduced the classification of cortical neurons as simple and complex on the basis of four tests of their receptive field structure. These tests are partly subjective and no one of them unequivocally places neurons into distinct classes. A simple, objective classification criterion based on the form of the response to drifting sinusoidal gratings has been used by several laboratories, although it has been criticized by others. We review published and unpublished evidence which indicates that this simple and objective criterion reliability divides neurons of the striate cortex in both cats and monkeys into two groups that correspond closely to the classically-described simple and complex classes.

Comparison of recordings from microelectrode arrays and single electrodes in the visual cortex

Advances in microelectrode neural recording systems have made it possible to record extracellular activity from a large number of neurons simultaneously. A substantial body of work is associated with traditional single-electrode extracellular recording, and the robustness of the recording method has

Inhibitory refinement of spatial frequency selectivity in single cells of the cat striate cortex.

Single cells in the cat striate cortex are more selective for the spatial frequency of sinewave grating stimuli than are cells of the retina or lateral geniculate nucleus. We have explored the possibility that this enhancement of selectivity results from spatial-frequency-selective inhibition. Stimulation with two superimposed gratings, one to excite the cell and one to prove for inhibition, revealed spatial frequency-dependent response suppression in 74% of the total population studied. Suppression was slightly more prevalent in simple cells (80%) than in complex cells (68%). In 93% of the cases where suppression was found, its tuning was complementary to excitatory spatial frequency tuning, and the strongest suppression was usually found where the excitatory tuning function approached zero imp./sec. Characteristics of the phenomenon were independent of cortical layers. We conclude that organized inhibitory mechanisms serve to refine the spatial frequency bandpass of striate cortical cells. This provides evidence for another degree of nonlinearity in the organization of cortical receptive fields and supports the hypothesis that a fundamental function of the visual cortex is image dissection in the domain of spatial frequency.

Are primate lateral geniculate nucleus (LGN) cells really sensitive to orientation or direction

There is considerable controversy over the existence of orientation and direction sensitivity in lateral geniculate nucleus (LGN) neurons. Claims for the existence of these properties often were based upon data from cells tested well beyond their peak spatial frequencies. The goals of the present study were to examine the degree of orientation and direction sensitivity of LGN cells when tested at their peak spatial and temporal frequencies and to compare the tuning properties of these subcortical neurons with those of visual cortex. For this investigation, we used conventional extracellular recording to study orientation and direction sensitivities of owl monkey LGN cells by stimulating cells with drifting sinusoidal gratings at peak temporal frequencies, peak or higher spatial frequencies, and moderate contrast. A total of 110 LGN cells (32 koniocellular cells, 34 magnocellular cells, and 44 parvocellular cells) with eccentricities ranging from 2.6 deg to 27.5 deg were examined. Using the peak spatial and temporal frequencies for each cell, 41.8% of the LGN cells were found to be sensitive to orientation and 19.1% were direction sensitive. The degree of bias for orientation and direction did not vary with eccentricity or with cell class. Orientation sensitivity did, however, increase, and in some cases orientation preferences changed, at higher spatial frequencies. Increasing spatial frequency had no consistent effect on direction sensitivity. Compared to cortical cell orientation tuning, the prevalence and strength of LGN cell orientation and direction sensitivity are weak. Nevertheless, the high percentage of LGN cells sensitive to orientation even at peak spatial and temporal frequencies reinforces the view that subcortical biases could, in combination with activity-dependent cortical mechanisms and/or cortical inhibitory mechanisms, account for the much narrower orientation and direction tuning seen in visual cortex.

Deconstruction of Spatial Integrity in Visual Stimulus Detected by Modulation of Synchronized Activity in Cat Visual Cortex

Spatiotemporal relationships among contour segments can influence synchronization of neural responses in the primary visual cortex. We performed a systematic study to dissociate the impact of spatial and temporal factors in the signaling of contour integration via synchrony. In addition, we characterized the temporal evolution of this process to clarify potential underlying mechanisms. With a 10 × 10 microelectrode array, we recorded the simultaneous activity of multiple cells in the cat primary visual cortex while stimulating with drifting sine-wave gratings. We preserved temporal integrity and systematically degraded spatial integrity of the sine-wave gratings by adding spatial noise. Neural synchronization was analyzed in the time and frequency domains by conducting cross-correlation and coherence analyses. The general association between neural spike trains depends strongly on spatial integrity, with coherence in the gamma band (35–70 Hz) showing greater sensitivity to the change of spatial structure than other frequency bands. Analysis of the temporal dynamics of synchronization in both time and frequency domains suggests that spike timing synchronization is triggered nearly instantaneously by coherent structure in the stimuli, whereas frequency-specific oscillatory components develop more slowly, presumably through network interactions. Our results suggest that, whereas temporal integrity is required for the generation of synchrony, spatial integrity is critical in triggering subsequent gamma band synchronization.

Visual resolution and sensitivity in a nocturnal primate (galago) measured with visual evoked potentials

Visual resolution and contrast sensitivity were examined in anesthetized, paralyzed galagos using visual evoked potentials (VEPs) resulting from stimulation with phase-reversed sinewave gratings. Spatial frequency vs contrast response functions were band-pass with peak sensitivity at 0.2-0.4 c/deg and a high frequency cut-off between 1.6 and 3 c/deg. Peak contrast sensitivities (estimated from extrapolation of contrast response functions) varied across animals from 10 to 170. Variation of the stimulus modulation rate showed that best responses occurred at 1 Hz with an upper limit of 6-16 Hz. As in other primates, an oblique effect was seen in 6 of 8 animals. The contrast sensitivity function (CSF) determined from cortical VEPs agrees well with the CSFs of cells in the lateral geniculate nucleus, but peak sensitivity and spatial frequency are slightly lower than found for the behavioral CSF. Overall visual performance resembled closely that of another nocturnal species, the cat.

Contrast adaptation in striate cortical neurons of the nocturnal primate bush baby ( Galago crassicaudatus)

It has been argued that in order for the visual system to detect edges accurately under a range of conditions, the visual system needs to adapt to the local contrast level to preserve sensitivity (Blakemore & Campbell, 1969). Cells in the primary visual cortex of cats adapt to stimuli with low to moderate contrast. Curiously, macaque monkey neurons in primary visual cortex (V1) do not show evidence for similar adaptation. To address the question of whether this differential sensitivity in contrast adaptation might be due to phylogenetic variation between cats and primates or to specializations for visual niche (e.g. nocturnal vs. diurnal), contrast adaptation to temporally and spatially optimized gratings was examined in 30 V1 cells of three nocturnal primate bush babies (Galago crassicaudatus). A second objective was to examine the relationship between the degree of contrast adaptation and cell classification or cell location relative to cortical layers or compartments [i.e. cytochrome-oxidase (CO) blobs and interblobs]. All cells were classified (simple vs. complex) and anatomically localized relative to cortical layers and cytochrome-oxidase (CO) blob and interblob compartments. Two independent measures of contrast adaptation were used. In the first test, contrast was sequentially increased from 3-56% and then decreased. The contrast required to maintain a half-maximum response amplitude in the 30 cells tested increased an average of 0.24 (+/- 0.12) log units during the sequential decrements in contrast. For the second test, four sets of five interleaved contrasts within +/- 1 octave of a central adapting contrast (10%, 14%, 20%, and 28%, respectively) were presented. The cells produced a mean adaptation index of 0.57 (+/- 0.47) which is very similar to that exhibited by cat cortical neurons (0.54 +/- 0.41). Interestingly, cells in interblobs showed a trend toward greater adaptation than did blob cells. Moreover, cells in the supragranular layers exhibited greater adaptation than cells in the infragranular layers. No significant differences in adaptation were found to correlate with other cell classification indices. Taken together, our results suggest that contrast adaptation may be more important for maintaining sensitivity in nocturnal species (primates or cats) than in diurnal species (macaque monkeys), and that in the nocturnal bush baby, cells in cortical layers and compartments may be differentially specialized for contrast adaptation.

VISUAL EVOKED POTENTIAL RESPONSES OF THE ANESTHETIZED CAT TO CONTRAST MODULATION OF GRATING PATTERNS

Contrast modulation affords independent control of static contrast (C) and changes in contrast (delta C). We found that in anesthetized, paralyzed cats, the visual evoked potential (VEP) was dependent only on magnitude of delta C at each pattern transition, and was independent of the starting or ending contrast level. Increasing modulation frequency to above 2 Hz reduced the VEP monotonically, implying that the time constant for differentiation by the VEP is of the order of 250 msec. The essentially perfect a.c. coupling suppresses standing contrast completely, permitting the full dynamic range of the VEP response system to be used for detection of contrast increments (which results in a decreasing Weber fraction). The difference between our results and those of behavioral studies using contrast modulation can be explained by eye movements present in the behavioral studies which refresh the retinal image of the static contrast in a way uncorrelated to temporal modulation of the stimulus, thus introducing a masking effect.

Spike train analysis reveals cooperation between Area 17 neuron pairs that enhances fine discrimination of orientation

We recorded from 22 pairs of neurons neurons in cats anesthetized with Propofol and N2O and paralyzed with Pavulon following established guidelines. We used type analysis (Johnson et al., 2001) to calculate the Resistor Average Kullback-Leibler distance between ensemble responses to fine ( 10deg, >0.1c/deg) variations of OR and SF from the optimal parameter (see panel below). This “distance” provides an estimate of the reduction in classification error between responses (i.e., reduction in error = 2-distance). Discharge history was incorporated into types by testing for a stable Markov order (i.e., where discharge history ceases to contribute) using conditional types on previous bins for distance calculations. PURPOSE Bursting in Area 17 is tuned more sharply than spike rate for orientation (OR) and spatial frequency (SF) (Cattaneo et al., 1981a,b). Burst length is reduced at non-optimal orientations (DeBusk et al., 1997) and leads to less efficient synaptic coupling (Snider et al., 1998). We describe how these interspike interval (ISI) properties could contribute to discriminations between spike trains for fine and gross differences in OR and SF. We also describe changes in neural dependency as a function of OR, SF, contrast, and time to demonstrate how cooperative information (synergy) arises and is transmitted.

Relationships between the spatiotemporal structure of spike trains and cortical synchronization

There remains considerable uncertainty about the underlying causes and functional significance of cortical oscillation and synchronization. We examined the temporal structure and synchronization of spikes in cell assemblies (groups of 4-6 cells with similar orientation preference). Recordings were made with a 5x5 microelectrode array in supragranular layers of Area 17 of cats paralyzed and anesthetized with propofol and N 2 O. Auto-correlograms (rate-normalized) of 24 single-unit recordings reveal burst (100%) and oscillatory (63%) firing. The average bursting interval was 2.9 ms and the average frequency of oscillation was 49.8 Hz. Results from renewal density analysis, used to explore the source of oscillation, suggest that it arises mainly from extrinsic influences such as feedback. However, a bursting refractory period, presumably intrinsic, could also encourage oscillatory firing. When we investigated the source of synchronization for 60 cell pairs we only found moderate correlation of synchrony with bursts and oscillation. We did, nonetheless, discover a possible functional role for oscillation. In all cases of cross-correlograms that exhibited oscillation, the strength of the synchrony was maintained throughout the stimulation period. When no oscillation was apparent, 75% of the cell pairs had some decay in synchronization. We propose that structured input, which results in tight organization of latency, is a more likely candidate than oscillation for the source of synchronization. The latency differences between cell pairs (R 2 = 0.50), as well as the SD of the differences (R 2 = 0.53) were logarithmically correlated with the synchronization. The reliable synchrony at response onset could be driven by the spatial and temporal correlations of the stimulus preserved through the earlier stages of the visual system. Oscillation helps to maintain the synchrony to enhance reliable transmission of the information for higher cognitive processing.