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In This Article

  • Summary
  • Abstract
  • Introduction
  • Protocol
  • Results
  • Discussion
  • Disclosures
  • Acknowledgements
  • Materials
  • References
  • Reprints and Permissions

Summary

Temporal processing, a preattentive process, may underlie deficits in higher-level cognitive processes, including attention, commonly observed in neurocognitive disorders. Using prepulse inhibition as an exemplar paradigm, we present a protocol for manipulating interstimulus interval (ISI) to establish the shape of the ISI function to provide an assessment of temporal processing.

Abstract

Temporal processing deficits have been implicated as a potential elemental dimension of higher-level cognitive processes, commonly observed in neurocognitive disorders. Despite the popularization of prepulse inhibition (PPI) in recent years, many current protocols promote using a percent of control measure, thereby precluding the assessment of temporal processing. The present study used cross-modal PPI and gap prepulse inhibition (gap-PPI) to demonstrate the benefits of employing a range of interstimulus intervals (ISIs) to delineate effects of sensory modality, psychostimulant exposure, and age. Assessment of sensory modality, psychostimulant exposure, and age reveals the utility of an approach varying the interstimulus interval (ISI) to establish the shape of the ISI function, including increases (sharper curve inflections) or decreases (flattening of the response amplitude curve) in startle amplitude. Additionally, shifts in peak response inhibition, suggestive of a differential sensitivity to the manipulation of ISI, are often revealed. Thus, the systematic manipulation of ISI affords a critical opportunity to evaluate temporal processing, which may reveal the underlying neural mechanisms involved in neurocognitive disorders.

Introduction

Temporal processing deficits have been implicated as a potential underlying neural mechanism for alterations in higher-level cognitive processes commonly observed in neurocognitive disorders. Prepulse inhibition (PPI) of the auditory startle response (ASR) is a translational experimental paradigm commonly used to examine temporal processing deficits, revealing profound alterations in neurocognitive disorders such as schizophrenia1, attention deficit hyperactivity disorder2 and HIV-1 associated neurocognitive disorders3,4. Specifically, assessments of temporal processing in preclinical models of HIV-1 have revealed the generality, relative permanence, and suggested the diagnostic utility of PPI across the majority of the animals' functional lifespan3,4,5,6.

Use of an approach varying interstimulus interval (ISI; i.e., the time between the prepulse and the startle stimulus) in the analysis of reflex modification dates back to Sechenov in 18637. The seminal studies of reflex modification, a measure of sensorimotor gating, employed an approach varying ISI to assess flexor response and audition in frogs7,8, as well as knee-jerk responses in humans9. The first clinical application of the reflex modification procedure assessed visual sensitivity in a man with hysterical blindness10. Over a century after the first reports of reflex modification, the approach of varying ISI was popularized across a series of seminal papers11,12,13. Despite the inherent differences in the seminal studies on reflex modification (i.e., species, experimental procedures, reflexes), they established a temporal relationship that was strikingly similar between species.

Assessment of prepulse inhibition using an approach varying ISI, as detailed in the present protocol, has multiple advantages over the popularized percent of control approach. First, the approach affords an opportunity to establish the shape of the ISI function, including increases (sharper curve inflections) or decreases (flattening of the response amplitude curve)3,15 in startle amplitude, as well as shifts in the peak point of response inhibition3,5. Additionally, when an approach varying ISI is employed, startle response is a relatively stable phenomenon1, suggesting the potential utility of the approach in longitudinal studies examining the progression of neurocognitive deficits5,15. Finally, PPI provides a critical opportunity to understand the underlying neural circuitry involved in neurocognitive disorders16.

In our study, we employed two experimental paradigms (Figure 1), including cross-modal PPI and gap prepulse inhibition (gap-PPI), to evaluate the utility of an approach varying ISI to delineate effects of sensory modality, psychostimulant exposure, and age. The cross-modal PPI experimental paradigm utilizes the presentation of an added stimulus (e.g., tone, light, air puff) as a discrete prestimulus prior to an acoustic startling stimulus. In sharp contrast, in the gap-PPI experimental paradigm, the absence of a background (e.g., removal of background noise, light, or air puff) serves as a discrete prestimulus. Here, we describe both experimental paradigms for the assessment of temporal processing, as well as statistical approaches for the analysis of PPI and gap-PPI. Within the discussion, we compared the conclusions one would draw from the variable ISI approach and the popularized percent of control approach.

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Protocol

All animal protocols were reviewed and approved by the Animal Care and Use Committee at the University of South Carolina (federal assurance number: D16-00028).

1. Defining Parameters and Calibration of the Startle Apparatus

  1. Set up the startle response system (see Table of Materials) according to the manufacturer’s instructions.
    1. Enclose the startle platform in a 10 cm-thick double-walled isolation cabinet.
  2. Calibrate the response sensitivities using the startle calibration system.
  3. Attach the high-frequency loudspeaker 30 cm above the animal holder.
    1. Measure and calibrate the loudspeaker using a sound level meter by placing the microphone inside the animal holder.
  4. Affix a white LED light (22 lux) on the wall in front of the animal holder.
    1. Measure the lux presented as a visual prepulse using a light meter.
  5. Connect a semi-rigid plastic tube (0.64 mm diameter) to a compressed air tank via an airline regulator.
    1. Set the air tank to 16 psi for the presentation of tactile prestimuli.
    2. Use a sound level meter to measure the amount of noise being emitted by the tactile stimulus inside the tube, 2.5 cm from the end of the animal holder. If using multiple chambers, ensure that all chambers are calibrated in the same manner.
      Note: To prevent the tactile stimulus from being perceived as an acoustic stimulus, the sound of the air puff prepulse must be less than or equal to the white noise background. In the present set-up, the air puff prepulse emitted 70 db(A) inside the tube while the background white noise was also set to 70 db(A).

2. Creation of Experimental Programs

  1. Open the Startle Response System software (see Table of Materials).
  2. Click Definitions and Select Define Trial.
  3. Define a pulse-only ASR trial.
    Note: The pulse-only ASR trial is run during the habituation session, and 6 times at the beginning of every cross-modal PPI and gap-PPI session for habituation.
    1. Type a Trial Name. Hit Enter.
    2. Record Data.
    3. Set the Analog Level to 720.
    4. Define the Wait Length as 20 ms.
    5. Introduce Background.
    6. End the Trial.
    7. Hit Accept to save the trial.
  4. Click Definitions and Select Define Trial. 
  5. Create six separate trial definitions for acoustic PPI, including one trial for each ISI (i.e., 0, 30, 50, 100, 200, 4000 ms).
    1. Create a trial definition for the 0 ms ISI for acoustic PPI.
      1. Type a Trial Name. Hit Enter.
      2. Record Data.
      3. Set the Analog Level to 720.
      4. Assign the Wait Length to 20 ms.
      5. Introduce Background.
      6. End the Trial.
      7. Hit Accept to save the trial.
    2. Create remaining trial definitions for ISIs with both a prestimulus and a stimulus (i.e., 30, 50, 100, 200, 4000 ms).
      1. Type a Trial Name. Hit Enter.
      2. Set the Analog Level to 600 at 0 ms to introduce the prestimulus.
      3. Assign the Wait Length to 20 ms to specify the length of the prestimulus.
      4. Set the Analog Level to 440 at 20 ms to remove the prestimulus.
      5. Define the Wait Length dependent upon ISI.
        Note: Define the wait length as: 10 ms for the 30 ms ISI, 30 ms for the 50 ms ISI, 80 ms for the 100 ms ISI, 180 ms for the 200 ms ISI, and 3980 ms for the 4000 ms ISI. Only one wait length is included for each ISI.
      6. Record Data.
      7. Set the Analog Level to 720.
      8. Assign the Wait Length to 20 ms.
      9. Introduce Background.
      10. End the Trial.
      11. Hit Accept to save the trial.
  6. Click Definitions and Select Define Trial. 
  7. Create six separate trial definitions for visual or tactile PPI, including one trial for each ISI (i.e., 0, 30, 50, 100, 200, 4000 ms).
    1. Create a trial definition for the 0 ms ISI for visual or tactile PPI.
      1. Type a Trial Name. Hit Enter.
      2. Record Data.
      3. Turn the Tactile on.
      4. Set the Analog Level to 720 and the Wait Length to 20 ms.
      5. Turn the Tactile off.
      6. Introduce Background.
      7. End the Trial.
      8. Hit Accept to save the trial.
    2. Create remaining trial definitions for ISIs with both a prestimulus and a stimulus (i.e., 30, 50, 100, 200, 4000 ms).
      Note: Visual and tactile can not be run concurrently because of software and hardware limitations. The modality presented is dependent upon the input into the hardware (i.e., whether the light is connected or the air puff is connected).
      1. Type a Trial Name. Hit Enter.
      2. Turn the Tactile on to introduce the prestimulus.
        Note: In this instance, tactile refers to the modality (i.e., either visual or air puff) that is connected to the hardware.
      3. Set the Wait Length to 20 ms.
      4. Turn the Tactile off to remove the prestimulus.
      5. Set the Analog Level to 440 at 20 ms.
      6. Define the Wait Length dependent upon ISI.
        Note: Define the wait length as: 10 ms for the 30 ms ISI, 30 ms for the 50 ms ISI, 80 ms for the 100 ms ISI, 180 ms for the 200 ms ISI, and 3980 ms for the 4000 ms ISI.
      7. Record Data.
      8. Set the Analog Level to 720.
      9. Assign the Wait Length to 20 ms.
      10. Introduce Background.
      11. End the Trial.
      12. Hit Accept to save the trial.
  8. Click Definitions and Select Define Trial.
  9. Create six separate trial definitions for acoustic gap-PPI, including one trial for each ISI (i.e., 0, 30, 50, 100, 200, 4000 ms).
    1. Create a trial definition for the 0 ms ISI for acoustic gap-PPI.
      1. Type a Trial Name. Hit Enter.
      2. Record Data.
      3. Set the Analog Level to 720 and the Wait Length to 20 ms.
      4. Introduce Background.
      5. End the Trial.
      6. Hit Accept to save the trial.
    2. Create remaining trial definitions for ISIs with both a prestimulus and a stimulus (i.e., 30, 50, 100, 200, 4000 ms).
      1. Type a Trial Name. Hit Enter.
      2. Set the Analog Level to 0 at 0 ms to introduce the prestimulus.
      3. Assign the Wait Length to 20 ms to specify the length of the prestimulus.
      4. Set the Analog Level to 440 at 20 ms to remove the prestimulus.
      5. Define the Wait Length dependent upon ISI.
        Note: Define the wait length as: 10 ms for the 30 ms ISI, 30 ms for the 50 ms ISI, 80 ms for the 100 ms ISI, 180 ms for the 200 ms ISI, and 3980 ms for the 4000 ms ISI.
      6. Record Data.
      7. Set the Analog Level to 720.
      8. Assign the Wait Length to 20 ms.
      9. Introduce Background.
      10. End the Trial.
      11. Hit accept to save the trial.
  10. Click Definitions and Select Define Trial. 
  11. Create six separate trial definitions for the visual or tactile gap-PPI, including one trial for each ISI (i.e., 0, 30, 50, 100, 200, 4000 ms).
    1. Create a trial definition for the 0 ms ISI for visual or tactile gap-PPI.
      1. Type a Trial Name. Hit Enter.
      2. Turn the Tactile on.
      3. Record Data.
      4. Set the Analog Level to 720 and the Wait Length to 20 ms.
      5. Introduce Background.
      6. End the Trial.
      7. Hit Accept to save the trial.
    2. Create remaining trial definitions for ISIs with both a prestimulus and a stimulus (i.e., 30, 50, 100, 200, 4000 ms). 
      1. Type a Trial Name. Hit Enter.
      2. Turn the Tactile on.
      3. Set the Analog Level to 0 ms.
      4. Turn the Tactile off.
      5. Set the Wait Length to 20 ms.
      6. Turn the Tactile on.
      7. Set the Analog Level to 440.
      8. Define the Wait Length dependent upon ISI.
        Note: Define the wait length as: 10 ms for the 30 ms ISI, 30 ms for the 50 ms ISI, 80 ms for the 100 ms ISI, 180 ms for the 200 ms ISI, and 3980 ms for the 4000 ms ISI.
      9. Record Data.
      10. Set the Analog Level to 720.
      11. Assign the Wait Length to 20 ms.
      12. Introduce Background.
      13. End the Trial.
      14. Hit accept to save the trial.
  12. Select Definitions and Define Session.
    1. Create a habituation session.
      1. Set the Background Analog Level to 440, the Number of Record Samples to 200 the Samples per Second to 2000, the Acclimation Period to 5 min, and the Sequence Repetitions to 36.
      2. Type 10 into the intertrial interval (ITI) list box.
      3. Click Add and select the pulse-only ASR trial.
      4. Click Save to save the habituation session.
  13. Select Definitions and Define Session.
  14. Define the session for Cross-Modal PPI.
    1. Set the Background Analog Level to 440, the Number of Record Samples to 200 the Samples per Second to 2000, the Acclimation Period to 5 min, and the Sequence Repetitions to 1.
    2. Define the intertrial interval (ITI) list.
      1. Type 10 into the first 5 ITI list boxes.
      2. Type a variable ITI (15-25 s) into the next 72 ITI list boxes, representing trials with a prestimulus.
    3. Click Add.
      1. Select the pulse-only ASR trial and load it 6 times for Trials 1-6.
      2. Create 6-trial blocks for each prestimulus modality using a Latin Square design (Table 1).
      3. Load the 6-trial blocks in an ABBA counterbalanced order of presentation (e.g., acoustic, visual, visual, acoustic, acoustic, etc.) for cross-modal PPI.
        Note: Each trial must be loaded individually.
        Note: Each cross-modal PPI session includes a total of 78 trials.
    4. Click Save to save the session.
  15. Select Definitions and Define Session.
    1. Define the session for Gap-PPI.
      1. Set the Background Analog Level to 440, the Number of Record Samples to 200 the Samples per Second to 2000, the Acclimation Period to 5 min, and the Sequence Repetitions to 1.
      2. Define the intertrial interval (ITI) list.
        1. Type 10 into the first 5 ITI list boxes.
        2. Type a variable ITI (15-25 s) into the next 36 ITI list boxes, representing trials with a prestimulus.
      3. Click Load to load the trials.
        1. Select the pulse-only ASR trial and load it 6 times for Trials 1-6.
        2. Create 6-trial blocks for each prestimulus modality using a Latin Square design (Table 1).
      4. Click Save to save the session.
        Note: Each gap-PPI session includes a total of 42 trials. Each session assesses one sensory modality.

3. Protocol Structure

  1. Use the F344/N rat strain, the most common inbred rat strain, for assessments.
    Note: Cross-modal PPI and gap-PPI can be conducted in animals at a variety of ages, of both sexes, and regardless of hormonal status (i.e., ovariectomized, castrated, intact). Details regarding the animals used in the representative data are presented in the representative results.
  2. Handle the animals to allow for acclimation across a series of days prior to beginning experimentation.
  3. Randomize the order of animals for experimentation dependent upon the between-subjects’ factors of interest (e.g., biological sex, treatment).
  4. Open the startle response system software. Click Run. Select the session of interest.
    Note: Only one session is conducted per day and sessions need to be conducted in a sequential order (i.e., Habituation, Cross-Modal PPI, Gap-PPI)
  5. Input an Output File Name and click OK.
  6. Enter Subject, Group, and ID information and click Continue.
  7. Place the animal into the startle apparatus using an animal enclosure that is most appropriate for the size of the animal. Click OK to begin the session.
  8. Export data for analysis.
    1. Click Reports | Concatenate Data. Load the data file and click Add. Click ASCII to save the data output.

4. Data Analysis

  1. Calculate an adjusted V. Max for each trial by subtracting the V. Max from the Start value.
    Note: The adjusted V. Max creates a measure of mean peak ASR amplitude.
  2. Graphically visualize results for the habituation session.
    1. Plot group means and standard errors of the mean for each trial. Regression analyses can be conducted and fit with 95% confidence intervals.
  3. Graphically visualize results for cross-sectional cross-modal PPI and gap-PPI.
    1. Calculate mean values for each ISI by averaging across the 6 trials individually for each animal.
    2. Calculate and graph group means and standard errors of the mean for each ISI and sensory modality.
  4. Statistically analyze cross-modal PPI and gap-PPI (Optional).
    Note: Although the precise statistical approach will be dependent upon the experimental design and research question of interest, a mixed-design repeated measures ANOVA provides one appropriate approach.

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Results

A prominent non-monotonic ISI function was observed in cross-modal PPI (Figures 2A, 3A, 4A) and gap-PPI (Figures 2B, 3B, 4B). Baseline startle responses were observed at the 0 and 4000 ms ISIs, included as reference trials within a test session. The importance of the 4000 ms ISI cannot be understated, as it most closely resembles the PPI test trials (i.e., 30, 50, 100, 200 ms ISIs) in that the subject receives both the prepulse and startling stim...

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Discussion

The present protocol describes the power of varying ISI for the assessment of temporal processing for studies employing either cross-sectional or longitudinal experimental designs. Examining the effects of sensory modality, psychostimulant exposure, or age on the shape of the ISI function demonstrated its utility in revealing a differential sensitivity to the manipulation of ISI (i.e., shifts in the point of maximal inhibition) or a relative insensitivity to the manipulation of ISI (i.e., sharper inflec...

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Disclosures

None of the authors have conflicts of interest to declare.

Acknowledgements

This work was supported in part by grants from NIH (National Institute on Drug Abuse, DA013137; National Institute of Child Health and Human Development HD043680; National Institute of Mental Health, MH106392; National Institute of Neurological Diseases and Stroke, NS100624) and the interdisciplinary research training program supported by the University of South Carolina Behavioral-Biomedical Interface Program. Dr. Landhing Moran is currently a Scientific Officer at the NIDA Center for Clinical Trials Network.

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Materials

NameCompanyCatalog NumberComments
SR-Lab Startle Response SystemSan Diego Instruments
Isolation CabinetIndustrial Acoustic Company
SR-Lab Startle Calibration SystemSan Diego Instruments
High-Frequency LoudspeakerRadio Shackmodel #40-1278B
Sound Level MeterBruel & Kjaermodel #2203
Perspex CylinderSan Diego InstrumentsIncluded with the SR-Lab Startle Response System
SR-Lab Startle Response System SoftwareSan Diego InstrumentsIncluded with the SR-Lab Startle Response System
Light MeterSper Scientific, Ltd.model #840006
Airline RegulatorCraftsmanmodel #16023
SPSS Statistics 24IBMUsed for Statistical Analyses (Optional)

References

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Interstimulus IntervalTemporal ProcessingNeurocognitive DisordersCross sectional AssessmentLongitudinal AssessmentStartle Response SystemAcoustic PPINeurocircuitry AlterationsTrial DefinitionBackground Analog LevelHabituation SessionRecord Data

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