Assessing fear learning via conditioned respiratory amplitude responses

Abstract

Respiratory physiology is influenced by cognitive processes. It has been suggested that some cognitive states may be inferred from respiration amplitude responses (RAR) after external events. Here, we investigate whether RAR allow assessment of fear memory in cued fear conditioning, an experimental model of aversive learning. To this end, we built on a previously developed psychophysiological model (PsPM) of RAR, which regards interpolated RAR time series as the output of a linear time invariant system. We first establish that average RAR after CS+ and CS− are different. We then develop the response function of fear‐conditioned RAR, to be used in our PsPM. This PsPM is inverted to yield estimates of cognitive input into the respiratory system. We analyze five validation experiments involving fear acquisition and retention, delay and trace conditioning, short and medium CS‐US intervals, and data acquired with bellows and MRI‐compatible pressure chest belts. In all experiments, CS+ and CS− are distinguished by their estimated cognitive inputs, and the sensitivity of this distinction is higher for model‐based estimates than for peak scoring of RAR. Comparing these data with skin conductance responses (SCR) and heart period responses (HPR), we find that, on average, RAR performs similar to SCR in distinguishing CS+ and CS−, but is less sensitive than HPR. Overall, our work provides a novel and robust tool to investigate fear memory in humans that may allow wide and straightforward application to diverse experimental contexts.

Psychophysiological modeling: Current state and future directions

“…External events cause responses in these three measures that are captured with LTI systems, but as yet it is not clear which psychological states could be inferred from these responses (Bach, Gerster, Tzovara, & Castegnetti, ). In contrast, we have shown in several experiments that a CS + in fear conditioning elicits a biphasic respiratory amplitude response that can be modeled in a LTI system, thus allowing GLM inversion (Castegnetti et al, ) (see Equation and parameters for RAR_FC). The approach and its interpretation are similar to that for pupil size and heart period.…”

“…This bradycardia response appears to be added to a stimulus‐specific HPR that occurs for both CS + and CS‐ in fear conditioning, similar to what is observed for pupil size and with the same limitations for interpretation of response estimates. However, different from pupil responses, it appears to be time‐locked to the US when the CS‐US interval is varied (Castegnetti, Tzovara, Staib, Gerster, & Bach, ; Castegnetti et al, ). Furthermore, relating the bradycardia response to the first response component elicited by short stimuli revealed a putative neural input that peaks at the US (Castegnetti et al, ).…”

“…The fidelity of inference on fear memory has been demonstrated in several data sets but requires independent confirmation from different laboratories. Castegnetti et al () have suggested that fear‐conditioned bradycardia could potentially be—at least partly—induced by increased thorax pressure induced via respiration amplitude responses; this may be another interesting avenue of research.…”

“…It appears that fear memory can be inferred from respiration amplitude responses, and predictive validity of this inference is higher for a GLM inversion than peak scoring (Castegnetti et al, ); however, it is lower than for many other psychophysiological measures. A distinct advantage of the respiratory PsPM could be that it only requires single‐chest belt data, which is standardly available in many MRI scanners.…”

Critical evaluation of current data analysis strategies for psychophysiological measures of fear conditioning and extinction in humans

“…Whereas skin conductance is an index primarily of arousal, fearpotentiated startle is sensitive to both valence and arousal, meaning that it is useful for a wider breadth of less invasive stimuli, such as images (Lang, 1995). Indeed, of the measures routinely employed, skin conductance and fear-potentiated startle appear to index fear extinction most sensitively (Jovanovic, Norrholm, Sakoman, Esterajher, & Kozarić-Kovačić, 2009); however, there is recent evidence for possible uses of measurements of pupil dilation (Korn, Staib, Tzovara, Castegnetti, & Bach, 2017), bradycardia (Castegnetti et al, 2016) and respiration (Castegnetti, Tzovara, Staib, Gerster, & Bach, 2017).…”