Fig 1.
Schematic diagram of the EmGate model.
A–C, The model consists of three interacting maps: a sensory map (A), a salience map (B), and a plan map (C). The sensory map (A) and the plan map (C) are instantiations of the basic cortex-TRN-thalamus circuit shown in Inset D. This circuit enables competition between parallel cortico-thalamic loops (green excitatory projections). Each loop can inhibit all others through off-surround inhibition mediated by the TRN (red inhibitory projections). In the sensory map (A), this competition is equivalent to selective attention. In the plan map (C) this competition is equivalent to decision-making. The salience map (B) is the amygdala circuit, which represents sensory stimuli that acquire affective salience. Two subpopulations of LA and BA neurons (green excitatory neurons) exist in the salience map (B): one devoted to labeling appetitive stimuli (blue rectangle), and one devoted to labeling aversive stimuli (pink rectangle). Synaptic connection weights linking sensory thalamus with the feed-related LA subpopulation are enhanced when sensory thalamic activity co-occurs with food-related reinforcement signal R1 (in B and Inset E). Similarly, synaptic connection weights linking sensory thalamus with the fear-related LA subpopulation are enhanced when sensory thalamic activity co-occurs with fear-related signal R2. LA conveys salient sensory signals to BA, which communicates bidirectionally with the plan map (C). Each BA subpopulation sends converging signals to the corresponding plan loop, providing ‘evidence’ in support of the corresponding plan. Each BA subpopulation also receives top-down projections from the corresponding plan cortex neuron. Connections between plan cortex and BA are also strengthened by the reinforcement signals Rq (R1 or R2; in B and Inset E). The local amygdala circuit is shown in Inset E. Each BA neuron receives inhibition from a local interneuron that is excited by two signals: fast expectation confirmation (EC) and slower expectation violation (EV). The EC signal also inhibits EV preventing it from building up. The EC and EV signals are dependent on LA activity and reinforcement signals. The local plan cortical circuit is shown in Inset F. Each plan cortical neuron also receives inhibition from a local interneuron. The EC and EV signals in cortex are computed locally based on plan cortex activity and reinforcement signals. Each plan cortical neuron also receives a top-down motivation or biasing signal, Mq (M1 or M2 in Inset F). The two sources of inhibition in the Plan and Salience Map local circuits that are driven by local EC and EV signals can interrupt persistent positive excitatory feedback, allowing the system to reset itself and remain sensitive to changing contingencies. The expectation represented by each LA neuron is stimulus-specific and the expectation represented by each plan cortical neuron is plan-specific. Stimulus specificity is lost at the level of the Plan Map because all BA signals within a subpopulation converge onto a single plan loop, providing a summed excitation to the corresponding plan cortex, plan TRN and plan thalamus neurons. The BA neurons project to the sensory map (A), cortex (CTX), TRN and thalamus (Thal), biasing the competition among sensory loops in favor of stimuli that have been labeled by LA as salient. This allows the amygdala to bias attention to sensory signals with affective salience.
Fig 2.
Attentional suppression and selection by the EmGate model.
A, When the feed plan is active, only CS1 and CS2 can pass through the attentional gate (i) and (ii), but CS3 is suppressed via the BA-TRN projection (iii). B, When the fear plan is active, CS1 and CS2 are suppressed (i), (ii) and CS3 is attended to (iii). Note that LA neurons are only active when the corresponding CS is present [A(i), A(ii), B(iii)]. By contrast, BA neurons receive excitation from plan cortex, which allows the BA-TRN projection to mediate suppression of distractors and irrelevant stimuli even when the corresponding CS is not present. The subplots on the left show the behavior of the model when CS1 is presented (i). The subplots in the center show the behavior of the model when CS2 is presented (ii). The subplots on the right show the behavior of the model when CS3 is presented (iii).
Fig 3.
Slow flexible modulation of attention by emotion.
Each simulation is divided into 4 epochs (bottom): two conditioning phases, followed by two testing phases. Each subplot shows the time evolution of key model activities. A, Plan map. B, Salience map for appetitive (positive) stimuli. C, Salience map for aversive (negative) stimuli. D, E, F, Sensory map, including sensory cortex (D), sensory TRN sector (E) and sensory thalamus (F). G, Input to sensory thalamus (stimuli and distractors). H, Reinforcement signals and Conditioned Stimuli (CSs). Amplitudes of CSs are scaled down to 0.5 for visibility (H). In B-G, the y-axis represents the neuron index (neuron #); white indicates zero activity, and dark red/black indicates high activity. In A and H, the y-axis represents activity. In all subplots the x-axis represents time. During the first conditioning phase, CS1 and CS2 are associated with a food reward. During the second conditioning phase, CS3 is associated with an aversive stimulus. During both testing phases, the conditioned stimuli are presented repeatedly in the sequence CS1-CS3-CS2-CS3, with no reinforcement. Elevated activity of a sensory cortical neuron (D) corresponds to attention allocated to the corresponding stimulus (H). Elevated activity in an amygdalar BA principal neuron in a given subpopulation (B and C) represents the affective salience of the corresponding stimulus (H). Elevated activity in a plan cortical neuron (A) indicates that the corresponding behavioral plan is activated. During the testing phases, the rate at which the plan (A) shifts from feed (blue) to fear (red) is dependent on the rate of build-up of the plan cortical expectation violation (EV) signal. Here the cortical expectation violation signal builds up slowly in comparison with Fig 4, allowing each plan (A) to persist for some time despite stimulus-specific violations of expectation. In the bottom-up mode (green arrows), which depends on external stimuli, processing in the salience map (B, C) can (1) determine affective salience, focusing and shifting attention in the sensory map (D-F), and (2) provide evidence in support of plans corresponding to appetitive or aversive stimuli, driving decision-making and switching between the feed (blue plot) and fear (red plot) plan (A).
Fig 4.
Rapid flexible modulation of attention by emotion.
Axis and subplot labels are as in Fig 3. A, Plan map. B, Salience map for appetitive (positive) stimuli. C, Salience map for aversive (negative) stimuli. D, E, F, Sensory map, including sensory cortex (D), sensory TRN sector (E) and sensory thalamus (F). G, Input to sensory thalamus (stimuli and distractors). H, Reinforcement signals and Conditioned Stimuli (CSs). During the testing phases, the rate at which the plan (A) shifts from feed (blue) to fear (red) is dependent on the rate of build-up of the plan cortical expectation violation (EV) signal. Here the cortical expectation violation (EV) signal builds up rapidly in comparison with Fig 3, causing the plan to shift after a single expectation violation (A). The speed of resetting of cortical plan representations (A) determines how often there is a temporal window of opportunity for bottom-up emotion-related signals (green arrows, B and C) to determine plans (A) and sensory attention (D, F).
Fig 5.
Focused top-down attention on food-related stimuli.
Axis and subplot labels are as in Fig 3. A, Plan map. B, Salience map for appetitive (positive) stimuli. C, Salience map for aversive (negative) stimuli. D, E, F, Sensory map, including sensory cortex (D), sensory TRN sector (E) and sensory thalamus (F). G, Input to sensory thalamus (stimuli and distractors). H, Reinforcement signals and Conditioned Stimuli (CSs). The simulations reveal that the amygdala-TRN projection can mediate both bottom-up (green arrows) and top-down (purple arrows) modulation of attention by emotion. During the first conditioning phase, CS1 and CS2 are associated with a food reward. During the second conditioning phase, CS3 is associated with an aversive stimulus. During the first testing phase (similar to Fig 3), the conditioned stimuli are presented repeatedly in the sequence CS1-CS3-CS2-CS3, with no reinforcement (bottom-up mode, green arrows). During testing phase 1, the rate at which the plan (A) shifts from feed (blue) to fear (red) is dependent on the rate of build-up of the plan cortical expectation violation (EV) signal. Here the cortical expectation violation signal builds up slowly (similar to Fig 3), allowing each plan (A) to persist for some time despite stimulus-specific violations of expectation. However, during the second testing phase (to the right of the vertical dotted line) top-down bias is applied to the feed plan (A–blue plot). This allows the feed plan to overcome the effects of expectation violation (EV), and remain active (in this simulation M1 = 160 during the second testing phase). Top-down excitation of BA neurons (purple arrow) allows BA (B) to direct attention only to the stimuli that were previously associated with food: CS1 and CS2. Attention to CS3 (D, F) is attenuated, despite the fact that it has been labeled as salient by virtue of its association with an aversive stimulus. Top-down cortical biasing (A) of BA can restrict attention to a particular category of affectively salient stimuli without restricting attention to only one stimulus. In other words, the system can divide attention between CS1 and CS2. Thus, even when the plan itself is locked in place by the top-down bias, there is within-plan flexibility to shift sensory attention. This flexibility arises because expectation violation signals cause inhibition of BA neurons.
Fig 6.
Focused top-down attention on fear-related stimuli.
Axis and subplot labels are as in Fig 5. A, Plan map. B, Salience map for appetitive (positive) stimuli. C, Salience map for aversive (negative) stimuli. D, E, F, Sensory map, including sensory cortex (D), sensory TRN sector (E) and sensory thalamus (F). G, Input to sensory thalamus (stimuli and distractors). H, Reinforcement signals and Conditioned Stimuli (CSs). The simulations reveal that the amygdala-TRN projection can mediate both bottom-up (green arrows) and top-down (purple arrows) modulation of attention by emotion. During the second testing phase (to the right of the vertical dotted line) top-down bias is applied to the fear plan. This allows the fear plan (A–red plot) to overcome the effects of inhibition elicited by expectation violation (EV) and remain active (in this simulation M2 = 160 during the second testing phase). Top-down excitation of BA neurons (purple arrows) allows BA (C) to restrict sensory attention to the stimulus that was previously associated with an aversive stimulus: CS3. Attention to CS1 and CS2 is attenuated (D, F), despite the fact that they have been labeled as salient.
Fig 7.
Impaired decision-making flexibility in the absense of inhibitory interneurons in plan cortex.
Axis and subplot labels are as in Fig 5. A, Plan map. The plan cortical inhibitory interneurons are 'lesioned' in the simulation. B, Salience map for appetitive (positive) stimuli. C, Salience map for aversive (negative) stimuli. D, E, F, Sensory map, including sensory cortex (D), sensory TRN sector (E) and sensory thalamus (F). G, Input to sensory thalamus (stimuli and distractors). H, Reinforcement signals and Conditioned Stimuli (CSs). During the second testing phase (to the right of the vertical dotted line) top-down bias is applied to the feed plan. The plans (A) cannot shift as in the previous simulations. Thus in the absense of inhibition onto the plan cortical neurons (triggered by expectation confirmation and violation), the decision-making flexibility of the system is degraded. (In this simulation M1 = 160 during the second testing phase).
Fig 8.
Attentional flexibility is impaired in the absense of BA inhibitory interneurons.
Axis and subplot labels are as in Fig 5. A, Plan map. B, C, Salience map. The BA interneurons are ‘lesioned’ in the simulation. D, E, F, Sensory map, including sensory cortex (D), sensory TRN sector (E) and sensory thalamus (F). G, Input to sensory thalamus (stimuli and distractors). H, Reinforcement signals and Conditioned Stimuli (CSs). During the second testing phase (to the right of the vertical dotted line) top-down bias is applied to the feed plan. The plans (A) shift as in the previous simulations, but within the periods when the feed plan (blue plot) is active, sensory attention (D) does not shift between the two relevant stimuli, CS1 and CS2. Attentional flexibility of the system is thus degraded in the absense of inhibition onto the BA neurons (triggered by stimulus-specific expectation violation). During the first testing phase, the rate at which the plan shifts from feed to fear is dependent on the rate of build-up of the cortical expectation violation signal. A slow build-up is employed, as in Fig 3. (In this simulation M1 = 160 during the second testing phase).
Fig 9.
Inflexibility in the absense of both BA interneurons and plan cortical interneurons.
Axis and subplot labels are as in Fig 5. A, Plan map. The plan cortical interneurons are ‘lesioned’ in the simulation. B, C, Salience map. The BA interneurons are ‘lesioned’ in the simulation. D, E, F, Sensory map, including sensory cortex (D), sensory TRN sector (E) and sensory thalamus (F). G, Input to sensory thalamus (stimuli and distractors). H, Reinforcement signals and Conditioned Stimuli (CSs). When the interneurons in BA and plan cortex are 'lesioned' the simulation reveals inability of the network to reset the cortical plan signals (A) as well as the sensory attentional modulation from BA (B, C), leading to pathological inflexibility in both attention (D, F) and decision-making (A). During the second testing phase (to the right of the vertical dotted line) top-down bias is applied to the feed plan. (In this simulation M1 = 160 during the second testing phase).
Fig 10.
Contributions of cortical and amygdalar interneurons to flexible decision-making and attention: Spiking model.
Time evolution of a key spiking model activity, during the first two seconds of the first testing phase. Simulations and key activities of the rate-coded and spiking models were similar, with each simulation divided into 4 epochs: two conditioning phases, followed by two testing phases. A, Cortical activity corresponding to the feed plan. B, Cortical activity corresponding to the fear plan. Plan cortical inhibitory interneurons (black spikes) trigger resetting of the corresponding plan (blue and red spikes), allowing a new plan to be selected. C, D, Activity in the salience map corresponding to appetitive (positive) stimuli (CS1, CS2). E, Activity in the salience map corresponding to an aversive (negative) stimulus (CS3). Amygdalar inhibitory interneurons (black spikes) trigger resetting of the corresponding BA principal neuron (green spikes), allowing a new CS to be selected if it is relevant to the ongoing plan (C-E). F, Activity in sensory cortex corresponding to CS1 (cyan), CS2 (orange), and CS3 (magenta). G, Conditioned Stimuli reaching sensory thalamus (CSs). In A-E, the inhibitory interneuron spiking activity is shown in black.
Fig 11.
A, B, Time evolution of the activity of the sensory cortical neurons corresponding to the target stimulus S1 (blue lines) and to the target stimulus S2 (pink lines) in the short lag (C) or long lag (D) condition. C, D, Presence of stimuli S1 (blue) and S2 (pink), separated by a short (A) or long (B) lag. The stimulus S1 was previously paired with an aversive US. If the time lag between the salient stimulus S1 and the target stimulus S2 is short (A, C), S1 causes suppression of representations of S2 via the amygdala-TRN pathway. If the time lag between the salient stimulus S1 and the target stimulus S2 is long (B, D), the inhibition triggered by S1 does not persist long enough to suppress S2. A stimulus is assumed to be detected if its cortical representation (A, B) crosses the variable detection threshold (black lines). Five detection trials out of a total of twenty are shown. The detection success rate for the short lag was 10%, and for the long lag was 100%. In all subplots the x-axis represents time and the y-axis represents amplitude.
Table 1.
Model neural activities.
Table 2.
Parameter values for the rate-coded model.
Table 3.
Parameter values for the spiking model.