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Region-specific effects of ultrasound on individual neurons in the awake mammalian brain

Hua-an Tseng, Jack Sherman, Emma Bortz, Ali Mohammed, Howard J. Gritton, Seth Bensussen, Rockwell P. Tang, Dana Zemel, Thomas Szabo, Xue Han

iScience 2021, 24, 102955 · 10.1016/j.isci.2021.102955

rodenthealthycellular imaging

Abstract

Ultrasound modulates brain activity. However, it remains unclear how ultrasound affects individual neurons in the brain, where neural circuit architecture is intact and different brain regions exhibit distinct tissue properties. Using a high-resolution calcium imaging technique, we characterized the effect of ultrasound stimulation on thousands of individual neurons in the hippocampus and the motor cortex of awake mice. We found that brief 100-ms-long ultrasound pulses increase intracellular calcium in a large fraction of individual neurons in both brain regions. Ultrasound-evoked calcium response in hippocampal neurons exhibits a rapid onset with a latency shorter than 50 ms. The evoked response in the hippocampus is shorter in duration and smaller in magnitude than that in the motor cortex. These results demonstrate that noninvasive ultrasound stimulation transiently increases intracellular calcium in individual neurons in awake mice, and the evoked response profiles are brain region specific.

Abstract via europepmc.

Speciesmouse (C57BL/6)
Subjects14, 4swept animals
Sessions per subjectnot reported
Randomisednot reported
Blindingnot reported
Sham / controlinactive transducer, active control site
Auditory controlnot reported
Readout timingonline
Anaesthesiaawake
Readoutscellular imagingLarge-scale single-neuron GCaMP6f/jGCaMP7f calcium imaging (wide-field fluorescence microscope, 20 Hz)
Direction of effectexcitatoryUltrasound reliably increased intracellular calcium (GCaMP6 fluorescence) in a large fraction of individual neurons in both hippocampal CA1 and motor cortex; responses in motor cortex were larger in amplitude and longer in duration than in hippocampus.
Adverse eventsnot reported

Exposures

Exposure 1: Ultrasound stimulation of hippocampal CA1 during calcium imaging in awake mice

Target: CA1 — “hippocampus CA1
Device: other named manufacturer · The Ultra Group Inc · GS350-D13 (planar ultrasound transducer)

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)350✓✓
Pulse duration (ms)0.214✓✓
Pulse repetition frequency (Hz)2,000✓✓
Duty cycle (%)not reportedpulse duration × PRF gives 42.8%
Sonication duration (s)0.1✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)440✓✓
Free-field Isppa (W/cm²)not reported
Free-field Ispta (W/cm²)not reported
In-situ estimatesimulationsingle value
In-situ pressure (kPa)24.3✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

During each imaging session, mice experienced 20 trials of ultrasound stimulation, each trial lasting 30 or 60 s, with ultrasound onset 10 s after start of imaging. Each stimulation consisted of 200 pulses at 2 kHz, each pulse containing 75 cycles of 350 kHz sine wave ultrasound, for a total 100-ms-long stimulation period, delivered via a planar transducer placed under the animal's head.

Exposure 2: Ultrasound stimulation of motor cortex during calcium imaging in awake mice

Target: motor cortex — “motor cortex
Device: other named manufacturer · The Ultra Group Inc · GS350-D13 (planar ultrasound transducer)

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)350✓✓
Pulse duration (ms)0.214✓✓
Pulse repetition frequency (Hz)2,000✓✓
Duty cycle (%)not reportedpulse duration × PRF gives 42.8%
Sonication duration (s)0.1✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)440✓✓
Free-field Isppa (W/cm²)not reported
Free-field Ispta (W/cm²)not reported
In-situ estimatesimulationsingle value
In-situ pressure (kPa)26.3✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

Following the same protocol as the hippocampal experiments, mice experienced 20 trials of 30 or 60 s each, with ultrasound onset 10 s after imaging start. Each stimulation consisted of 200 pulses at 2 kHz, each pulse containing 75 cycles of 350 kHz sine wave ultrasound, for a total 100-ms-long stimulation period, delivered via a planar transducer placed under the animal's head; an off-target control positioned the transducer under the abdomen instead.

Flags from extraction

  • exposures[*].timing.pulse_duration_msComputed as cycles-per-pulse divided by fundamental frequency (75 cycles / 350 kHz = 0.214 ms), which the extraction instructions list as an allowed unit conversion rather than prohibited arithmetic.
  • n_subjectsPaper never gives one aggregate subject count; reported group sizes for the two brain-region ultrasound exposures are given as a list (14 mice for hippocampus, 4 mice for motor cortex). Separate sham (3 mice) and off-target abdomen-control (5 mice) groups are not included since they did not receive on-target ultrasound.
  • exposures[0].in_situ.pressure_kpaExact number (24.3 kPa) appears in the source text but the sentence is split awkwardly across a figure-caption insertion in the extracted markdown; quoted the sentence fragment containing the number as it appears verbatim.