On the importance of the transient visual response in the superior colliculus
Introduction
A friend waves to you from across the room. Your eyes respond to this visual motion by sending a signal directly, or indirectly via the cortex, to cells in the superior colliculus (SC) – a hub of sensory and motor processing in the middle of the brain. Some of these SC cells may already be at a heightened level of activity because you were scanning the crowd looking for her. The transient visual signal initiated by her wave arrives on these neurons to drive them over threshold to initiate a visual grasp reflex (visueller Greifreflex [1, 2]) – a rapid shift of gaze to align the high acuity retinal fovea with her face. Along with this overt orienting of gaze there are momentary changes in heart rate, blood pressure and brain wave activity, that are all part of a global orienting reflex that will prepare your body for possible action [3].
SC (optic tectum in non-mammals) circuitry and function is highly conserved phylogenetically [4, 5, 6, 7], and the transient visual response in the SC is a rich, spatial signal, the properties of which determines the latency of orienting responses to visual targets [8, 9, 10]. Recent research has shown that this is owing to a unique convergence of inputs and processes that modulate this transient response, and by how this signal is broadcast to the rest of the brain through diverse connections with cortex, basal ganglia, and muscles that drive orienting responses. Here, we argue that this transient visual response in the SC has access to the appropriate inputs, intrinsic processing features, and outputs to generate and distribute a signal related to the behavioral priority of an event (after [11••]). By ‘priority’ we mean the convergence of bottom–up salience (i.e. stimulus related) information with the top–down relevance an event has for the observer based on expectations and prior experience.
Section snippets
The transient visual signal is generated by neurons with the appropriate input structure
Figure 1 highlights important brain areas involved in the orienting network that have been identified and reviewed in detail elsewhere [6, 7, 11••, 12, 13, 14, 15]. The SC is a critical hub in this circuit. It is a multi-layered structure (Figure 2a) that can be separated functionally into superficial, visual-only layers (SCs), and intermediate and deep layers (SCi) receiving convergent sensory, cognitive, and motor inputs. Visual inputs to the SCs arise from retina indirectly via the
The transient visual signal represents the when and where, but not the what
A priority signal cannot be exhaustive in what it represents. Ideally, it should mark the time, place, and priority of the event as a tag to be sent to other brain areas focused on processing stimulus features [11••]. The transient visual signal in the SC is constrained to an orderly spatial map (Figure 3a), and is of short-latency owing to its direct input from the earliest stages of visual processing. It is dependent on factors influencing the physical distinctiveness (salience) of the
The transient visual signal can cause fast action directly
Under evolutionary pressure, a priority signal would be required to stimulate immediate action, either towards stimuli of interest (e.g. prey) or away from perilous stimuli (e.g. large looming things). The SC mediates these two fast responses through access to different motor output channels [4, 5]. Unlike other parts of the visual orienting network (see Figure 1), the visuomotor output neurons of the SCi have direct projections to the premotor circuitry in the brainstem and spinal cord to
The transient visual signal is modulated by cortical and basal ganglia inputs
A priority signal ought to have inputs which can increase or decrease its magnitude when priority changes. The incoming transient visual signal builds upon baseline activity in SCi neurons that can be very high if there is strong expectation, motor preparation, and/or reward signals [32] that emerge via reduced inhibition from substantia nigra par reticulata (SNr) in the basal ganglia, and/or through enhanced excitatory inputs from frontal or parietal cortex. The baseline can be very low if
The transient visual signal is influenced by other senses
The transient response would not be of much use as a global signal of event priority if it only responded to visual stimuli. Within the SCi there are well known auditory and somatosensory inputs whose reference frames are transformed to be in register with the retinotopic representation [7]. When these auditory and tactile signals are spatiotemporally congruent, they can also merge with the visual transient to raise its magnitude and shorten saccade latencies [35].
The transient visual signal reduces with repetition
Stimuli that are repetitive will decrease in novelty, causing the repeating stimulus to lose priority. The simplest way the brain has to track this is via sensory adaptation [36] or habituation [37], whereby stimulus repetition without consequence reduces response magnitude. Visual responses in both the SCs and SCi [38] diminish with even a single stimulus repetition, and the reduction in the signal is sufficient to delay saccadic reaction time [9, 11••, 39, 40]. This phenomenon also occurs in
The transient visual signal has the correct output structure to distribute a priority signal
For a priority signal to be useful it must have direct access to other brain regions that require that information. Through its extensive connections to extrastriate, parietal and frontal cortex via the pulvinar [47, 48] and anterior thalamus [49], and via direct connections to the basal ganglia, and brainstem circuitry controlling action, the SC is poised to distribute its spatially constrained priority signal to almost all systems (Figure 1). Even when no action is taken towards a salient
The transient visual signal is projected to the reinforcement learning circuitry in the basal ganglia
It is important for a priority signal to provide input to the reinforcement learning circuitry so that the organism can learn about the novel stimuli generated by their actions. If those actions are rewarded, they will be repeated and the resultant stimulus may change in priority. Recently it has been shown that the visual transient in the SCi is projected monosynaptically [55] to the dopaminergic neurons of the substantia nigra pars compacta in the basal ganglia (Figure 1). The transient
Conclusions
We have proposed that the transient visual response in the SC contains the appropriate input structure, intrinsic processing features, and distribution network to be the source of a priority signal [11••] that marks the onset of important events. This transient signal may also represent the substrate of covert orienting – the obligatory ‘noticing’ of a stimulus in the periphery without actually shifting gaze towards it. Important processing related to signal priority is observed in many places,
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
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