Silencing "Top-Down" Cortical Signals Affects Spike-Responses of Neurons in Cat's "Intermediate" Visual Cortex

Abstract

We examined the effects of reversible inactivation of a higher-order, pattern/form-processing, postero-temporal visual (PTV) cortex on the background activities and spike-responses of single neurons in the ipsilateral cytoarchitectonic area 19 (putative area V3) of anesthetized domestic cats. Very occasionally (2/28), silencing recurrent "feedback" signals from PTV, resulted in significant and reversible reduction in background activity of area 19 neurons. By contrast, in large proportions of area 19 neurons, PTV inactivation resulted in: (i) significant reversible changes in the peak magnitude of their responses to visual stimuli (35.5%; 10/28); (ii) substantial reversible changes in direction selectivity indices (DSIs; 43%; 12/28); and (iii) reversible, upward shifts in preferred stimulus velocities (37%; 7/19). Substantial (≥20°) shifts in preferred orientation and/or substantial (≥20°) changes in width of orientation-tuning curves of area 19 neurons were however less common (26.5%; 4/15). In a series of experiments conducted earlier, inactivation of PTV also induced upward shifts in the preferred velocities of the ipsilateral cytoarchitectonic area 17 (V1) neurons responding optimally at low velocities. These upward shifts in preferred velocities of areas 19 and 17 neurons were often accompanied by substantial increases in DSIs. Thus, in both the primary visual cortex and the "intermediate" visual cortex (area 19), feedback from PTV plays a modulatory role in relation to stimulus velocity preferences and/or direction selectivity, that is, the properties which are usually believed to be determined by the inputs from the dorsal thalamus and/or feedforward inputs from the primary visual cortices. The apparent specialization of area 19 for processing information about stationary/slowly moving visual stimuli is at least partially determined, by the feedback from the higher-order pattern-processing visual area. Overall, the recurrent signals from the higher-order, pattern/form-processing visual cortex appear to play an important role in determining the magnitude of spike-responses and some "motion-related" receptive field properties of a substantial proportion of neurons in the intermediate form-processing visual area-area 19.

Keywords: area V3; feedback from higher-order cortices; infero-temporal cortex; peristriate cortex; reversible inactivation.

Figure 1

(A) The dorsolateral view of cat’s left cerebral hemisphere with approximate location of electrode penetrations in area 19. Upward arrow indicates approximate position of the Horsley-Clarke anterior-posterior zero coordinates. Dark gray area indicates the location of the foot of the cooling probe which covered most of areas 20a and 20b. Lighter gray indicates the spread of cooling in the vicinity of cooling foot. (B) A block diagram of the cat’s visual system with simplified neuronal circuitry of retino-geniculo-cortical pathways, pattern/form and motion processing cortico-cortical hierarchies. Note that many cortical areas including area 19 and postero-temporal visual (PTV) cortex are directly interconnected via horizontal cortico-cortical feedforward and feedback connections (after Rosenquist, ; Dreher, ; Salin and Bullier, ; Scannell et al., ; Dreher et al., 1996). (C) The location of receptive field (RF) centers of 28 area 19 neurons tested for the effects of cooling of PTV. Note the location of RF centers of 11 area 17 neurons examined for velocity-tuning in the previous series of experiments (Huang et al., 2007). (D) Outlines of RFs of area 19 neurons of two cats included in the present study. The effects of cooling PTV were tested only in some cells. The bottom right insert plots area 19 cells’ average RF areas at azimuths around 5° and 20°. (E) Frequency distribution of eye dominance classes of area 19 cells recorded in the present study (solid lines) and the cooling sample (red dotted lines). Area 17 data are shown in green.

Figure 2

(A) Peri-stimulus time histograms (PSTHs) of spike-responses of a class 2 complex area 19 cell, to optimally oriented bar moving at different velocities across it’s RF. Upper row—before cooling, middle row—during cooling and lower row—after rewarming. Note, the absence of background spike-activity in all conditions. (B) Effects of cooling on peak magnitudes (spikes/s) of visually evoked responses of an area 19 neuron whose responses are illustrated in (A). (C) Effects of cooling on visually evoked background spike-activities of area 19 neurons. Note that only in two cells (*) there was significant reduction. (D) The peak magnitudes of visually evoked responses before cooling PTV vs. those during cooling (i). (ii) Cells tested for velocity-tuning. (iii) Cells tested for orientation-tuning. A-pr and A-npr refer to responses of cell in Figure 3A at preferred and non-preferred directions respectively. Note that the same cell is represented twice. (iv) Responses after rewarming PTV—all but one cell exhibited significant recovery. # In (i, ii and iv) denote responses indicated by # in (B).

Figure 3

(Ai) PSTHs of spike-responses of an area 19 complex, class 2 cell, illustrating the influence of cooling of PTV on peak spike-responses to moving stimuli of two different orientations. Note that during PTV inactivation the cell exhibited substantial decrease in its peak responses to stimuli moving along the axis of one orientation (20°–200°) and a substantial increase in its peak responses to stimuli of another orientation (60°–240°). Stimulus size: 10° × 0.6°. (Aii) Effects of PTV cooling on orientation-tuning property of the same cell shown in (Ai). Note during cooling, there was a 40° shift in optimal orientation but only in the non-preferred direction of movements. The shift was accompanied by an increase in orientation-tuning width at half-height (WHH). Thirty minutes after PTV was rewarmed, the responses and optimal orientation recovered to the pre-cooling levels. (B) Optimal orientations prior to cooling vs. those during cooling(i—preferred direction, ii—non-preferred direction) or after rewarming of PTV (iii—preferred direction, iv—non-preferred direction). In the insert frequency histogram within (Bi), cells exhibiting large (≥20°) shifts in optimal orientation during inactivation of PTV are represented. Note that the numbers indicate the number of data points that overlap. (C) The widths of orientation-tuning curves at half-height calculated from the control condition vs. those during PTV cooling (i) and control condition vs. those after PTV rewarming (ii) * in (Ci) and (Cii) indicate a cell whose responses are illustrated in (Ai) and (Aii). A-pr and A-npr refer to responses of cell in panel (A) at preferred and non-preferred directions respectively. Note the same cell is represented twice. The responses in non-preferred direction is indicated by * -npr.

Figure 4

(A) Effects of PTV cooling on PSTHs of spike-responses of a class 2 complex area 19 cell to optimally oriented bar moving at different velocities. The stimulus was presented via the dominant (contralateral) eye. Stimulus size: 5° × 1°. (B) Velocity-tuning of peak spike-responses of the same cell whose responses are shown in (A). Note in (A,B) there is a substantial increase in the magnitude of responses during inactivation of PTV, especially for movement from left to right. (C) Preferred velocities of area 19 cells before inactivation vs. those during PTV inactivation (i) and control vs. rewarming (ii). In most cases, during cooling, inactivation resulted in upward shifts in preferred velocities. Note that the numbers indicate the number of data points that overlap. (Di) The direction selectivity indices (DSIs) of area 19 cells at stimulus velocities optimal before inactivation. In a large proportion of cells, inactivation resulted in large (≥20%) changes in their DSIs. Also in five cells (*) inactivation resulted in reversal of preferred directions of movements. # Denotes the response indicated by # in upper panel of (B). (Dii) DSIs at stimulus velocities optimal after PTV rewarming. @ Denotes the response indicated by @ in upper panel of (B). (Ei) The DSIs of a subpopulation of area 19 cells calculated at stimulus velocities optimal during cooling. Note in a majority of cells, inactivation resulted in large increases in their DSIs. (Eii) DSIs at stimulus velocities optimal during cooling in control condition vs. those after PTV rewarming.

Figure 5

(A) Effects of PTV cooling on PSTHs of spike-responses of a class 2 area 17 complex cell to optimally oriented light bar moving at different velocities. Stimulus size: 10° × 0.4°. Note the bin widths for PSTHs for stimulus velocities 6.6°/s, 19.8°/s and 33°/s were 22 ms while those for the velocity 46.2°/s, the bin width was 6 ms. (B) Velocity-tuning of peak spike-responses of the same cell shown in (A). Note that during PTV inactivation there is a substantial increase in the magnitude of responses as well as substantial increases in DSI especially at velocities of 6.6°/s and 19.8°/s. (C) Preferred velocities of area 17 cells before vs. those during cooling. Note also that in a couple of cells (a and b), PTV cooling resulted in upward shifts in the preferred velocities. Finally, note that the numbers indicate the number of data points that overlap. (D) Effects of PTV cooling on the magnitude of spike-responses of area 17 cells. ! In (C) and (D) denote the cell marked in lower panel of (B). (E) DSIs of area 17 cells at stimulus velocities optimal before cooling. Note in three cells, cooling PTV resulted in large (≥20%) changes in their DSIs. *Indicates cell in which inactivation of PTV resulted in complete reversal of preferred direction.